Fibroblastic reticular cells enhance T cell metabolism and survival via epigenetic remodeling

Lymph node fibroblastic reticular cells (FRCs) respond to signals from activated T cells by releasing nitric oxide, which inhibits T cell proliferation and restricts the size of the expanding T cell pool. Whether interactions with FRCs also support the function or differentiation of activated CD8 +...

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Veröffentlicht in:	Nature immunology Jg. 20; H. 12; S. 1668 - 1680
Hauptverfasser:	Brown, Flavian D., Sen, Debattama R., LaFleur, Martin W., Godec, Jernej, Lukacs-Kornek, Veronika, Schildberg, Frank A., Kim, Hye-Jung, Yates, Kathleen B., Ricoult, Stéphane J. H., Bi, Kevin, Trombley, Justin D., Kapoor, Varun N., Stanley, Illana A., Cremasco, Viviana, Danial, Nika N., Manning, Brendan D., Sharpe, Arlene H., Haining, W. Nicholas, Turley, Shannon J.
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	New York Nature Publishing Group US 01.12.2019 Nature Publishing Group
Schlagworte:	631/1647 631/250 Animals Biomedical and Life Sciences Biomedicine CD8 antigen CD8-Positive T-Lymphocytes - immunology Cell Differentiation Cell Proliferation Cell Survival Cells, Cultured Cellular Reprogramming Chromatin Chromatin Assembly and Disassembly Cytotoxicity, Immunologic Epigenesis, Genetic Epigenetic inheritance Epigenetics Fibroblasts - physiology Gene Expression Regulation Immunologic Memory Immunological memory Immunology Infectious Diseases Interleukin 6 Interleukin-6 - genetics Interleukin-6 - metabolism Interleukins Lymph nodes Lymph Nodes - immunology Lymphocyte Activation Lymphocytes Lymphocytes T Lymphoid tissue Memory cells Mice Mice, Inbred C57BL Mice, Knockout Nitric oxide Nitric Oxide - metabolism T cells Massachusetts
ISSN:	1529-2908, 1529-2916, 1529-2916
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Abstract	Lymph node fibroblastic reticular cells (FRCs) respond to signals from activated T cells by releasing nitric oxide, which inhibits T cell proliferation and restricts the size of the expanding T cell pool. Whether interactions with FRCs also support the function or differentiation of activated CD8 + T cells is not known. Here we report that encounters with FRCs enhanced cytokine production and remodeled chromatin accessibility in newly activated CD8 + T cells via interleukin-6. These epigenetic changes facilitated metabolic reprogramming and amplified the activity of pro-survival pathways through differential transcription factor activity. Accordingly, FRC conditioning significantly enhanced the persistence of virus-specific CD8 + T cells in vivo and augmented their differentiation into tissue-resident memory T cells. Our study demonstrates that FRCs play a role beyond restricting T cell expansion—they can also shape the fate and function of CD8 + T cells. Fibroblastic reticular cells (FRCs) are dynamic regulators of lymphoid tissue structure. Turley and colleagues show FRCs also support activated T cells by producing IL-6, which confers an advantage to CD8+ T cell memory responses.
AbstractList	Lymph node fibroblastic reticular cells (FRCs) respond to signals from activated T cells by releasing nitric oxide, which inhibits T cell proliferation and restricts the size of the expanding T cell pool. Whether interactions with FRCs also support the function or differentiation of activated CD8.sup.+ T cells is not known. Here we report that encounters with FRCs enhanced cytokine production and remodeled chromatin accessibility in newly activated CD8.sup.+ T cells via interleukin-6. These epigenetic changes facilitated metabolic reprogramming and amplified the activity of pro-survival pathways through differential transcription factor activity. Accordingly, FRC conditioning significantly enhanced the persistence of virus-specific CD8.sup.+ T cells in vivo and augmented their differentiation into tissue-resident memory T cells. Our study demonstrates that FRCs play a role beyond restricting T cell expansion--they can also shape the fate and function of CD8.sup.+ T cells. Lymph node fibroblastic reticular cells (FRCs) respond to signals from activated T cells by releasing nitric oxide, which inhibits T cell proliferation and restricts the size of the expanding T cell pool. Whether interactions with FRCs also support the function or differentiation of activated CD8.sup.+ T cells is not known. Here we report that encounters with FRCs enhanced cytokine production and remodeled chromatin accessibility in newly activated CD8.sup.+ T cells via interleukin-6. These epigenetic changes facilitated metabolic reprogramming and amplified the activity of pro-survival pathways through differential transcription factor activity. Accordingly, FRC conditioning significantly enhanced the persistence of virus-specific CD8.sup.+ T cells in vivo and augmented their differentiation into tissue-resident memory T cells. Our study demonstrates that FRCs play a role beyond restricting T cell expansion--they can also shape the fate and function of CD8.sup.+ T cells. Fibroblastic reticular cells (FRCs) are dynamic regulators of lymphoid tissue structure. Turley and colleagues show FRCs also support activated T cells by producing IL-6, which confers an advantage to CD8+ T cell memory responses. Lymph node fibroblastic reticular cells (FRCs) respond to signals from activated T cells by releasing nitric oxide, which inhibits T cell proliferation and restricts the size of the expanding T cell pool. Whether interactions with FRCs also support the function or differentiation of activated CD8+ T cells is not known. Here we report that encounters with FRCs enhanced cytokine production and remodeled chromatin accessibility in newly activated CD8+ T cells via interleukin-6. These epigenetic changes facilitated metabolic reprogramming and amplified the activity of pro-survival pathways through differential transcription factor activity. Accordingly, FRC conditioning significantly enhanced the persistence of virus-specific CD8+ T cells in vivo and augmented their differentiation into tissue-resident memory T cells. Our study demonstrates that FRCs play a role beyond restricting T cell expansion—they can also shape the fate and function of CD8+ T cells. Lymph node fibroblastic reticular cells (FRCs) respond to signals from activated T cells by releasing nitric oxide, which inhibits T cell proliferation and restricts the size of the expanding T cell pool. Whether interactions with FRCs also support the function or differentiation of activated CD8+ T cells is not known. Here we report that encounters with FRCs enhanced cytokine production and remodeled chromatin accessibility in newly activated CD8+ T cells via interleukin-6. These epigenetic changes facilitated metabolic reprogramming and amplified the activity of pro-survival pathways through differential transcription factor activity. Accordingly, FRC conditioning significantly enhanced the persistence of virus-specific CD8+ T cells in vivo and augmented their differentiation into tissue-resident memory T cells. Our study demonstrates that FRCs play a role beyond restricting T cell expansion—they can also shape the fate and function of CD8+ T cells.Fibroblastic reticular cells (FRCs) are dynamic regulators of lymphoid tissue structure. Turley and colleagues show FRCs also support activated T cells by producing IL-6, which confers an advantage to CD8+ T cell memory responses. Lymph node fibroblastic reticular cells (FRCs) respond to signals from activated T cells by releasing nitric oxide, which inhibits T cell proliferation and restricts the size of the expanding T cell pool. Whether interactions with FRCs also support the function or differentiation of activated CD8+ T cells is not known. Here we report that encounters with FRCs enhanced cytokine production and remodeled chromatin accessibility in newly activated CD8+ T cells via interleukin-6. These epigenetic changes facilitated metabolic reprogramming and amplified the activity of pro-survival pathways through differential transcription factor activity. Accordingly, FRC conditioning significantly enhanced the persistence of virus-specific CD8+ T cells in vivo and augmented their differentiation into tissue-resident memory T cells. Our study demonstrates that FRCs play a role beyond restricting T cell expansion-they can also shape the fate and function of CD8+ T cells.Lymph node fibroblastic reticular cells (FRCs) respond to signals from activated T cells by releasing nitric oxide, which inhibits T cell proliferation and restricts the size of the expanding T cell pool. Whether interactions with FRCs also support the function or differentiation of activated CD8+ T cells is not known. Here we report that encounters with FRCs enhanced cytokine production and remodeled chromatin accessibility in newly activated CD8+ T cells via interleukin-6. These epigenetic changes facilitated metabolic reprogramming and amplified the activity of pro-survival pathways through differential transcription factor activity. Accordingly, FRC conditioning significantly enhanced the persistence of virus-specific CD8+ T cells in vivo and augmented their differentiation into tissue-resident memory T cells. Our study demonstrates that FRCs play a role beyond restricting T cell expansion-they can also shape the fate and function of CD8+ T cells. Lymph node fibroblastic reticular cells (FRCs) respond to signals from activated T cells by releasing nitric oxide, which inhibits T cell proliferation and restricts the size of the expanding T cell pool. Whether interactions with FRCs also support the function or differentiation of activated CD8 T cells is not known. Here we report that encounters with FRCs enhanced cytokine production and remodeled chromatin accessibility in newly activated CD8 T cells via interleukin-6. These epigenetic changes facilitated metabolic reprogramming and amplified the activity of pro-survival pathways through differential transcription factor activity. Accordingly, FRC conditioning significantly enhanced the persistence of virus-specific CD8 T cells in vivo and augmented their differentiation into tissue-resident memory T cells. Our study demonstrates that FRCs play a role beyond restricting T cell expansion-they can also shape the fate and function of CD8 T cells. Lymph node fibroblastic reticular cells (FRCs) respond to signals from activated T cells by releasing nitric oxide, which inhibits T cell proliferation and restricts the size of the expanding T cell pool. Whether interactions with FRCs also support the function or differentiation of activated CD8 + T cells is not known. Here we report that encounters with FRCs enhanced cytokine production and remodeled chromatin accessibility in newly activated CD8 + T cells via interleukin-6. These epigenetic changes facilitated metabolic reprogramming and amplified the activity of pro-survival pathways through differential transcription factor activity. Accordingly, FRC conditioning significantly enhanced the persistence of virus-specific CD8 + T cells in vivo and augmented their differentiation into tissue-resident memory T cells. Our study demonstrates that FRCs play a role beyond restricting T cell expansion—they can also shape the fate and function of CD8 + T cells. Fibroblastic reticular cells (FRCs) are dynamic regulators of lymphoid tissue structure. Turley and colleagues show FRCs also support activated T cells by producing IL-6, which confers an advantage to CD8+ T cell memory responses.
Audience	Academic
Author	Godec, Jernej Cremasco, Viviana Lukacs-Kornek, Veronika Sharpe, Arlene H. Kim, Hye-Jung Trombley, Justin D. Turley, Shannon J. Stanley, Illana A. Danial, Nika N. Yates, Kathleen B. LaFleur, Martin W. Haining, W. Nicholas Manning, Brendan D. Brown, Flavian D. Bi, Kevin Ricoult, Stéphane J. H. Kapoor, Varun N. Sen, Debattama R. Schildberg, Frank A.
AuthorAffiliation	4 Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, USA 11 Department of Pathology, Brigham and Women’s Hospital, Boston, MA, USA 9 Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, MA, USA 10 Department of Cell Biology, Harvard Medical School, Boston, MA, USA 14 Present address: Institute of Experimental Immunology, University Hospital of the Rheinische Friedrich-Wilhelms-University, Bonn, Germany 16 Present address: Immuno-Oncology, Novartis Institutes for BioMedical Research, Cambridge, MA, USA 7 Department of Genetics and Complex Diseases, Harvard T.H. Chan School of Public Health, Boston, MA, USA 12 Division of Pediatric Hematology and Oncology, Children’s Hospital, Boston, MA, USA 2 Department of Pediatric Oncology, Dana-Farber Cancer Institute, Boston, MA, USA 6 Broad Institute of Harvard and Massachusetts Institute of Technology, Cambridge, MA, USA 15 Present address: Clinic for Orthopedics and Trauma Surger
AuthorAffiliation_xml	– name: 2 Department of Pediatric Oncology, Dana-Farber Cancer Institute, Boston, MA, USA – name: 8 Department of Cancer Immunology, Genentech, South San Francisco, CA, USA – name: 5 Department of Cancer Immunology and Virology, Dana-Farber Cancer Institute, Boston, MA, USA – name: 6 Broad Institute of Harvard and Massachusetts Institute of Technology, Cambridge, MA, USA – name: 10 Department of Cell Biology, Harvard Medical School, Boston, MA, USA – name: 15 Present address: Clinic for Orthopedics and Trauma Surgery, University Hospital Bonn, Bonn, Germany – name: 12 Division of Pediatric Hematology and Oncology, Children’s Hospital, Boston, MA, USA – name: 4 Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, USA – name: 13 Present address: Neon Therapeutics Inc., Cambridge, MA, USA – name: 1 Division of Medical Sciences, Harvard Medical School, Boston, MA, USA – name: 16 Present address: Immuno-Oncology, Novartis Institutes for BioMedical Research, Cambridge, MA, USA – name: 11 Department of Pathology, Brigham and Women’s Hospital, Boston, MA, USA – name: 9 Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, MA, USA – name: 14 Present address: Institute of Experimental Immunology, University Hospital of the Rheinische Friedrich-Wilhelms-University, Bonn, Germany – name: 3 Department of Microbiology and Immunobiology, Harvard Medical School, Boston, MA, USA – name: 17 Present address: Merck Research Laboratories, Boston, MA, USA – name: 7 Department of Genetics and Complex Diseases, Harvard T.H. Chan School of Public Health, Boston, MA, USA
Author_xml	– sequence: 1 givenname: Flavian D. surname: Brown fullname: Brown, Flavian D. organization: Division of Medical Sciences, Harvard Medical School, Department of Pediatric Oncology, Dana-Farber Cancer Institute, Department of Microbiology and Immunobiology, Harvard Medical School, Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Department of Cancer Immunology and Virology, Dana-Farber Cancer Institute, Neon Therapeutics Inc – sequence: 2 givenname: Debattama R. orcidid: 0000-0002-0947-8284 surname: Sen fullname: Sen, Debattama R. organization: Division of Medical Sciences, Harvard Medical School, Department of Pediatric Oncology, Dana-Farber Cancer Institute – sequence: 3 givenname: Martin W. orcidid: 0000-0002-5017-774X surname: LaFleur fullname: LaFleur, Martin W. organization: Division of Medical Sciences, Harvard Medical School, Department of Pediatric Oncology, Dana-Farber Cancer Institute, Department of Microbiology and Immunobiology, Harvard Medical School, Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital – sequence: 4 givenname: Jernej surname: Godec fullname: Godec, Jernej organization: Division of Medical Sciences, Harvard Medical School, Department of Pediatric Oncology, Dana-Farber Cancer Institute, Department of Microbiology and Immunobiology, Harvard Medical School, Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital – sequence: 5 givenname: Veronika surname: Lukacs-Kornek fullname: Lukacs-Kornek, Veronika organization: Department of Cancer Immunology and Virology, Dana-Farber Cancer Institute, Institute of Experimental Immunology, University Hospital of the Rheinische Friedrich-Wilhelms-University – sequence: 6 givenname: Frank A. orcidid: 0000-0003-0797-1945 surname: Schildberg fullname: Schildberg, Frank A. organization: Department of Microbiology and Immunobiology, Harvard Medical School, Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Department of Cancer Immunology and Virology, Dana-Farber Cancer Institute, Clinic for Orthopedics and Trauma Surgery, University Hospital Bonn – sequence: 7 givenname: Hye-Jung surname: Kim fullname: Kim, Hye-Jung organization: Department of Microbiology and Immunobiology, Harvard Medical School, Department of Cancer Immunology and Virology, Dana-Farber Cancer Institute – sequence: 8 givenname: Kathleen B. surname: Yates fullname: Yates, Kathleen B. organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Broad Institute of Harvard and Massachusetts Institute of Technology – sequence: 9 givenname: Stéphane J. H. surname: Ricoult fullname: Ricoult, Stéphane J. H. organization: Department of Genetics and Complex Diseases, Harvard T.H. Chan School of Public Health – sequence: 10 givenname: Kevin surname: Bi fullname: Bi, Kevin organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Broad Institute of Harvard and Massachusetts Institute of Technology – sequence: 11 givenname: Justin D. surname: Trombley fullname: Trombley, Justin D. organization: Department of Microbiology and Immunobiology, Harvard Medical School, Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital – sequence: 12 givenname: Varun N. surname: Kapoor fullname: Kapoor, Varun N. organization: Department of Cancer Immunology, Genentech – sequence: 13 givenname: Illana A. surname: Stanley fullname: Stanley, Illana A. organization: Department of Cancer Biology, Dana-Farber Cancer Institute, Department of Cell Biology, Harvard Medical School – sequence: 14 givenname: Viviana surname: Cremasco fullname: Cremasco, Viviana organization: Department of Cancer Immunology and Virology, Dana-Farber Cancer Institute, Immuno-Oncology, Novartis Institutes for BioMedical Research – sequence: 15 givenname: Nika N. surname: Danial fullname: Danial, Nika N. organization: Department of Cancer Biology, Dana-Farber Cancer Institute, Department of Cell Biology, Harvard Medical School – sequence: 16 givenname: Brendan D. surname: Manning fullname: Manning, Brendan D. organization: Department of Genetics and Complex Diseases, Harvard T.H. Chan School of Public Health – sequence: 17 givenname: Arlene H. orcidid: 0000-0002-9736-2109 surname: Sharpe fullname: Sharpe, Arlene H. email: arlene_sharpe@hms.harvard.edu organization: Department of Microbiology and Immunobiology, Harvard Medical School, Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Broad Institute of Harvard and Massachusetts Institute of Technology, Department of Pathology, Brigham and Women’s Hospital – sequence: 18 givenname: W. Nicholas orcidid: 0000-0001-7871-3762 surname: Haining fullname: Haining, W. Nicholas email: nick.haining@merck.com organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Broad Institute of Harvard and Massachusetts Institute of Technology, Division of Pediatric Hematology and Oncology, Children’s Hospital, Merck Research Laboratories – sequence: 19 givenname: Shannon J. orcidid: 0000-0002-0444-3031 surname: Turley fullname: Turley, Shannon J. email: turley.shannon@gene.com organization: Department of Cancer Immunology and Virology, Dana-Farber Cancer Institute, Department of Cancer Immunology, Genentech
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/31636464$$D View this record in MEDLINE/PubMed
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Copyright	The Author(s), under exclusive licence to Springer Nature America, Inc. 2019 COPYRIGHT 2019 Nature Publishing Group Copyright Nature Publishing Group Dec 2019 The Author(s), under exclusive licence to Springer Nature America, Inc. 2019.
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 F.D.B. conceived and conducted most of the experiments, analyzed and interpreted data and wrote the manuscript. D.R.S. conducted experiments and analyzed and interpreted data. J.G., M.W.L., V.L.-K., F.A.S., H-J.K., K.B.Y., S.J.H.R., K.B. and V.N.K. conducted experiments and interpreted data. J.D.T. and I.A.S. discussed data and provided technical assistance. V.C., N.N.D. and B.D.M. discussed and interpreted data. A.H.S., W.N.H. and S.J.T. directed the study, analyzed and interpreted results and wrote the manuscript. Author contributions
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PublicationTitle	Nature immunology
PublicationTitleAbbrev	Nat Immunol
PublicationTitleAlternate	Nat Immunol
PublicationYear	2019
Publisher	Nature Publishing Group US Nature Publishing Group
Publisher_xml	– name: Nature Publishing Group US – name: Nature Publishing Group
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Snippet	Lymph node fibroblastic reticular cells (FRCs) respond to signals from activated T cells by releasing nitric oxide, which inhibits T cell proliferation and...
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SubjectTerms	631/1647 631/250 Animals Biomedical and Life Sciences Biomedicine CD8 antigen CD8-Positive T-Lymphocytes - immunology Cell Differentiation Cell Proliferation Cell Survival Cells, Cultured Cellular Reprogramming Chromatin Chromatin Assembly and Disassembly Cytotoxicity, Immunologic Epigenesis, Genetic Epigenetic inheritance Epigenetics Fibroblasts - physiology Gene Expression Regulation Immunologic Memory Immunological memory Immunology Infectious Diseases Interleukin 6 Interleukin-6 - genetics Interleukin-6 - metabolism Interleukins Lymph nodes Lymph Nodes - immunology Lymphocyte Activation Lymphocytes Lymphocytes T Lymphoid tissue Memory cells Mice Mice, Inbred C57BL Mice, Knockout Nitric oxide Nitric Oxide - metabolism T cells
Title	Fibroblastic reticular cells enhance T cell metabolism and survival via epigenetic remodeling
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