TOX transcriptionally and epigenetically programs CD8+ T cell exhaustion
Exhausted CD8 + T (T ex ) cells in chronic infections and cancer have limited effector function, high co-expression of inhibitory receptors and extensive transcriptional changes compared with effector (T eff ) or memory (T mem ) CD8 + T cells. T ex cells are important clinical targets of checkpoint...
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| Vydáno v: | Nature (London) Ročník 571; číslo 7764; s. 211 - 218 |
|---|---|
| Hlavní autoři: | , , , , , , , , , , , , , , , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | angličtina |
| Vydáno: |
London
Nature Publishing Group UK
11.07.2019
Nature Publishing Group |
| Témata: | |
| ISSN: | 0028-0836, 1476-4687, 1476-4687 |
| On-line přístup: | Získat plný text |
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| Abstract | Exhausted CD8
+
T (T
ex
) cells in chronic infections and cancer have limited effector function, high co-expression of inhibitory receptors and extensive transcriptional changes compared with effector (T
eff
) or memory (T
mem
) CD8
+
T cells. T
ex
cells are important clinical targets of checkpoint blockade and other immunotherapies. Epigenetically, T
ex
cells are a distinct immune subset, with a unique chromatin landscape compared with T
eff
and T
mem
cells. However, the mechanisms that govern the transcriptional and epigenetic development of T
ex
cells remain unknown. Here we identify the HMG-box transcription factor TOX as a central regulator of T
ex
cells in mice. TOX is largely dispensable for the formation of T
eff
and T
mem
cells, but it is critical for exhaustion: in the absence of TOX, T
ex
cells do not form. TOX is induced by calcineurin and NFAT2, and operates in a feed-forward loop in which it becomes calcineurin-independent and sustained in T
ex
cells. Robust expression of TOX therefore results in commitment to T
ex
cells by translating persistent stimulation into a distinct T
ex
cell transcriptional and epigenetic developmental program.
The transcription factor TOX is a central regulator of the transcriptional and epigenetic development of exhausted T cells. |
|---|---|
| AbstractList | Exhausted CD8+ T cells (TEX) in chronic infections and cancer have limited effector function, high inhibitory receptor co-expression and extensive transcriptional changes compared to effector (TEFF) or memory (TMEM) CD8+ T cells. TEX are important clinical targets of checkpoint blockade and other immunotherapies. Epigenetically, TEX are a distinct immune subset, with a unique chromatin landscape compared to TEFF and TMEM. However, the mechanisms governing the transcriptional and epigenetic development of TEX remain unknown. Here, we identify the HMG-box transcription factor TOX as a central regulator of TEX. TOX is largely dispensable for TEFF and TMEM formation, but is critical for exhaustion and without TOX TEX do not form. TOX is induced by calcineurin and NFAT2 and operates in a feed-forward loop to become calcineurin independent and sustained in TEX. Thus, robust TOX expression results in commitment to TEX by translating persistent stimulation into a distinct TEX transcriptional and epigenetic developmental program. Exhausted CD8 + T (T ex ) cells in chronic infections and cancer have limited effector function, high co-expression of inhibitory receptors and extensive transcriptional changes compared with effector (T eff ) or memory (T mem ) CD8 + T cells. T ex cells are important clinical targets of checkpoint blockade and other immunotherapies. Epigenetically, T ex cells are a distinct immune subset, with a unique chromatin landscape compared with T eff and T mem cells. However, the mechanisms that govern the transcriptional and epigenetic development of T ex cells remain unknown. Here we identify the HMG-box transcription factor TOX as a central regulator of T ex cells in mice. TOX is largely dispensable for the formation of T eff and T mem cells, but it is critical for exhaustion: in the absence of TOX, T ex cells do not form. TOX is induced by calcineurin and NFAT2, and operates in a feed-forward loop in which it becomes calcineurin-independent and sustained in T ex cells. Robust expression of TOX therefore results in commitment to T ex cells by translating persistent stimulation into a distinct T ex cell transcriptional and epigenetic developmental program. The transcription factor TOX is a central regulator of the transcriptional and epigenetic development of exhausted T cells. Exhausted CD8+ T (Tex) cells in chronic infections and cancer have limited effector function, high co-expression of inhibitory receptors and extensive transcriptional changes compared with effector (Teff) or memory (Tmem) CD8+ T cells. Tex cells are important clinical targets of checkpoint blockade and other immunotherapies. Epigenetically, Tex cells are a distinct immune subset, with a unique chromatin landscape compared with Teff and Tmem cells. However, the mechanisms that govern the transcriptional and epigenetic development of Tex cells remain unknown. Here we identify the HMG-box transcription factor TOX as a central regulator of Tex cells in mice. TOX is largely dispensable for the formation of Teff and Tmem cells, but it is critical for exhaustion: in the absence of TOX, Tex cells do not form. TOX is induced by calcineurin and NFAT2, and operates in a feed-forward loop in which it becomes calcineurin-independent and sustained in Tex cells. Robust expression of TOX therefore results in commitment to Tex cells by translating persistent stimulation into a distinct Tex cell transcriptional and epigenetic developmental program. Exhausted CD8+ T (Tex) cells in chronic infections and cancer have limited effector function, high co-expression of inhibitory receptors and extensive transcriptional changes compared with effector (Teff) or memory (Tmem) CD8+ T cells. Tex cells are important clinical targets of checkpoint blockade and other immunotherapies. Epigenetically, Tex cells are a distinct immune subset, with a unique chromatin landscape compared with Teff and Tmem cells. However, the mechanisms that govern the transcriptional and epigenetic development of Tex cells remain unknown. Here we identify the HMG-box transcription factor TOX as a central regulator of Tex cells in mice. TOX is largely dispensable for the formation of Teff and Tmem cells, but it is critical for exhaustion: in the absence of TOX, Tex cells do not form. TOX is induced by calcineurin and NFAT2, and operates in a feed-forward loop in which it becomes calcineurin-independent and sustained in Tex cells. Robust expression of TOX therefore results in commitment to Tex cells by translating persistent stimulation into a distinct Tex cell transcriptional and epigenetic developmental program.Exhausted CD8+ T (Tex) cells in chronic infections and cancer have limited effector function, high co-expression of inhibitory receptors and extensive transcriptional changes compared with effector (Teff) or memory (Tmem) CD8+ T cells. Tex cells are important clinical targets of checkpoint blockade and other immunotherapies. Epigenetically, Tex cells are a distinct immune subset, with a unique chromatin landscape compared with Teff and Tmem cells. However, the mechanisms that govern the transcriptional and epigenetic development of Tex cells remain unknown. Here we identify the HMG-box transcription factor TOX as a central regulator of Tex cells in mice. TOX is largely dispensable for the formation of Teff and Tmem cells, but it is critical for exhaustion: in the absence of TOX, Tex cells do not form. TOX is induced by calcineurin and NFAT2, and operates in a feed-forward loop in which it becomes calcineurin-independent and sustained in Tex cells. Robust expression of TOX therefore results in commitment to Tex cells by translating persistent stimulation into a distinct Tex cell transcriptional and epigenetic developmental program. Exhausted CD8 T (T ) cells in chronic infections and cancer have limited effector function, high co-expression of inhibitory receptors and extensive transcriptional changes compared with effector (T ) or memory (T ) CD8 T cells. T cells are important clinical targets of checkpoint blockade and other immunotherapies. Epigenetically, T cells are a distinct immune subset, with a unique chromatin landscape compared with T and T cells. However, the mechanisms that govern the transcriptional and epigenetic development of T cells remain unknown. Here we identify the HMG-box transcription factor TOX as a central regulator of T cells in mice. TOX is largely dispensable for the formation of T and T cells, but it is critical for exhaustion: in the absence of TOX, T cells do not form. TOX is induced by calcineurin and NFAT2, and operates in a feed-forward loop in which it becomes calcineurin-independent and sustained in T cells. Robust expression of TOX therefore results in commitment to T cells by translating persistent stimulation into a distinct T cell transcriptional and epigenetic developmental program. |
| Author | Attanasio, John Mitchell, Tara C. Khan, Omar Giles, Josephine R. Kaye, Jonathan Werner, Michael T. Donahue, Greg Patel, Kunal P. Berger, Shelley L. Wherry, E. John Xu, Wei Amaravadi, Ravi K. Huang, Alexander C. Wu, Jennifer E. Karakousis, Giorgos C. Ngiow, Shin Foong Yan, Patrick George, Sangeeth M. Manne, Sasikanth Staupe, Ryan P. McDonald, Sierra Schuchter, Lynn M. Bengsch, Bertram Xu, Xiaowei Alexander, Katherine A. |
| AuthorAffiliation | 11 Research Division of Immunology, Department of Biomedical Sciences, Cedars-Sinai Medical Center, Los Angeles, CA USA 2 Institute for Immunology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA USA 4 Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA USA 8 Department of Pathology and Laboratory Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA USA 3 Parker Institute for Cancer Immunotherapy, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA USA 6 Department of Cell and Developmental Biology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA USA 9 Department of Medicine II, Gastroenterology, Hepatology, Endocrinology, and Infectious Diseases, University Medical Center Freiburg, Germany 10 BIOSS Centre for Biological Signaling Studies, Freiburg, Germany 1 Department of Systems Pharmacology and Translational Therapeutics, Perelman School of M |
| AuthorAffiliation_xml | – name: 7 Department of Genetics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA USA – name: 3 Parker Institute for Cancer Immunotherapy, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA USA – name: 9 Department of Medicine II, Gastroenterology, Hepatology, Endocrinology, and Infectious Diseases, University Medical Center Freiburg, Germany – name: 2 Institute for Immunology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA USA – name: 6 Department of Cell and Developmental Biology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA USA – name: 10 BIOSS Centre for Biological Signaling Studies, Freiburg, Germany – name: 8 Department of Pathology and Laboratory Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA USA – name: 5 Epigenetics Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA USA – name: 4 Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA USA – name: 11 Research Division of Immunology, Department of Biomedical Sciences, Cedars-Sinai Medical Center, Los Angeles, CA USA – name: 1 Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA USA |
| Author_xml | – sequence: 1 givenname: Omar surname: Khan fullname: Khan, Omar organization: Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Institute for Immunology, Perelman School of Medicine, University of Pennsylvania, Parker Institute for Cancer Immunotherapy, Perelman School of Medicine, University of Pennsylvania, Arsenal Biosciences – sequence: 2 givenname: Josephine R. surname: Giles fullname: Giles, Josephine R. organization: Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Institute for Immunology, Perelman School of Medicine, University of Pennsylvania, Parker Institute for Cancer Immunotherapy, Perelman School of Medicine, University of Pennsylvania – sequence: 3 givenname: Sierra surname: McDonald fullname: McDonald, Sierra organization: Epigenetics Institute, Perelman School of Medicine, University of Pennsylvania, Department of Cell and Developmental Biology, Perelman School of Medicine, University of Pennsylvania, Department of Genetics, Perelman School of Medicine, University of Pennsylvania – sequence: 4 givenname: Sasikanth surname: Manne fullname: Manne, Sasikanth organization: Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Institute for Immunology, Perelman School of Medicine, University of Pennsylvania – sequence: 5 givenname: Shin Foong surname: Ngiow fullname: Ngiow, Shin Foong organization: Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Institute for Immunology, Perelman School of Medicine, University of Pennsylvania, Parker Institute for Cancer Immunotherapy, Perelman School of Medicine, University of Pennsylvania – sequence: 6 givenname: Kunal P. surname: Patel fullname: Patel, Kunal P. organization: Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Institute for Immunology, Perelman School of Medicine, University of Pennsylvania, Department of Medicine, Perelman School of Medicine, University of Pennsylvania – sequence: 7 givenname: Michael T. surname: Werner fullname: Werner, Michael T. organization: Epigenetics Institute, Perelman School of Medicine, University of Pennsylvania, Department of Genetics, Perelman School of Medicine, University of Pennsylvania – sequence: 8 givenname: Alexander C. surname: Huang fullname: Huang, Alexander C. organization: Institute for Immunology, Perelman School of Medicine, University of Pennsylvania, Parker Institute for Cancer Immunotherapy, Perelman School of Medicine, University of Pennsylvania, Department of Medicine, Perelman School of Medicine, University of Pennsylvania – sequence: 9 givenname: Katherine A. surname: Alexander fullname: Alexander, Katherine A. organization: Epigenetics Institute, Perelman School of Medicine, University of Pennsylvania, Department of Cell and Developmental Biology, Perelman School of Medicine, University of Pennsylvania, Department of Genetics, Perelman School of Medicine, University of Pennsylvania – sequence: 10 givenname: Jennifer E. surname: Wu fullname: Wu, Jennifer E. organization: Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Institute for Immunology, Perelman School of Medicine, University of Pennsylvania, Parker Institute for Cancer Immunotherapy, Perelman School of Medicine, University of Pennsylvania – sequence: 11 givenname: John surname: Attanasio fullname: Attanasio, John organization: Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Institute for Immunology, Perelman School of Medicine, University of Pennsylvania – sequence: 12 givenname: Patrick surname: Yan fullname: Yan, Patrick organization: Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Institute for Immunology, Perelman School of Medicine, University of Pennsylvania – sequence: 13 givenname: Sangeeth M. surname: George fullname: George, Sangeeth M. organization: Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Institute for Immunology, Perelman School of Medicine, University of Pennsylvania – sequence: 14 givenname: Bertram surname: Bengsch fullname: Bengsch, Bertram organization: Department of Medicine II: Gastroenterology, Hepatology, Endocrinology, and Infectious Disease, University Medical Center Freiburg, BIOSS Centre for Biological Signaling Studies – sequence: 15 givenname: Ryan P. surname: Staupe fullname: Staupe, Ryan P. organization: Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Institute for Immunology, Perelman School of Medicine, University of Pennsylvania – sequence: 16 givenname: Greg surname: Donahue fullname: Donahue, Greg organization: Epigenetics Institute, Perelman School of Medicine, University of Pennsylvania, Department of Cell and Developmental Biology, Perelman School of Medicine, University of Pennsylvania, Department of Genetics, Perelman School of Medicine, University of Pennsylvania – sequence: 17 givenname: Wei surname: Xu fullname: Xu, Wei organization: Abramson Cancer Center, Perelman School of Medicine, University of Pennsylvania – sequence: 18 givenname: Ravi K. surname: Amaravadi fullname: Amaravadi, Ravi K. organization: Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Abramson Cancer Center, Perelman School of Medicine, University of Pennsylvania – sequence: 19 givenname: Xiaowei surname: Xu fullname: Xu, Xiaowei organization: Abramson Cancer Center, Perelman School of Medicine, University of Pennsylvania, Department of Pathology and Laboratory Medicine, Perelman School of Medicine, University of Pennsylvania – sequence: 20 givenname: Giorgos C. surname: Karakousis fullname: Karakousis, Giorgos C. organization: Abramson Cancer Center, Perelman School of Medicine, University of Pennsylvania, Department of Surgery, Perelman School of Medicine, University of Pennsylvania – sequence: 21 givenname: Tara C. surname: Mitchell fullname: Mitchell, Tara C. organization: Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Abramson Cancer Center, Perelman School of Medicine, University of Pennsylvania – sequence: 22 givenname: Lynn M. surname: Schuchter fullname: Schuchter, Lynn M. organization: Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Abramson Cancer Center, Perelman School of Medicine, University of Pennsylvania – sequence: 23 givenname: Jonathan surname: Kaye fullname: Kaye, Jonathan organization: Research Division of Immunology, Department of Biomedical Sciences, Cedars-Sinai Medical Center – sequence: 24 givenname: Shelley L. surname: Berger fullname: Berger, Shelley L. organization: Epigenetics Institute, Perelman School of Medicine, University of Pennsylvania, Department of Cell and Developmental Biology, Perelman School of Medicine, University of Pennsylvania, Department of Genetics, Perelman School of Medicine, University of Pennsylvania – sequence: 25 givenname: E. John surname: Wherry fullname: Wherry, E. John email: wherry@pennmedicine.upenn.edu organization: Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Institute for Immunology, Perelman School of Medicine, University of Pennsylvania, Parker Institute for Cancer Immunotherapy, Perelman School of Medicine, University of Pennsylvania |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31207603$$D View this record in MEDLINE/PubMed |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Lead Contact: E. John Wherry O.K. and E.J.W. conceived the project, designed experiments and wrote the manuscript. O.K. performed the majority of the experiments described herein and performed the in vitro, in vivo, and bioinformatics analysis. J.R.G. wrote the script to perform PSEA and, with S.M., performed pre-processing of RNA and ATAC-seq data. S.M. performed co-IP experiments for Western blot. S.F.N and K.P.P contributed to in vivo tumor and influenza experiments. M.T.W. performed IP experiments for mass spectrometry. A.C.H., P.Y., and S.M.G. acquired and stained human PBMC and TIL samples. J.E.W., R.P.S., and J.R.G. provided critical edits to the manuscript. All authors reviewed the manuscript. Contributions |
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| SSID | ssj0005174 |
| Score | 2.7246454 |
| Snippet | Exhausted CD8
+
T (T
ex
) cells in chronic infections and cancer have limited effector function, high co-expression of inhibitory receptors and extensive... Exhausted CD8 T (T ) cells in chronic infections and cancer have limited effector function, high co-expression of inhibitory receptors and extensive... Exhausted CD8+ T (Tex) cells in chronic infections and cancer have limited effector function, high co-expression of inhibitory receptors and extensive... Exhausted CD8+ T cells (TEX) in chronic infections and cancer have limited effector function, high inhibitory receptor co-expression and extensive... |
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| StartPage | 211 |
| SubjectTerms | 13 38 45 631/250/1619/554/1834 631/250/2152/1566 631/250/2152/1566/2493 631/250/2502/2170 631/250/255/2514 64/60 Animals Antigens Calcineurin Calcineurin - metabolism Calcium Signaling Cancer CD8 antigen CD8-Positive T-Lymphocytes - immunology CD8-Positive T-Lymphocytes - pathology Chromatin Cloning Epigenetics Epistasis, Genetic Exhaustion Feedback, Physiological Female Gene expression Gene Expression Regulation - immunology Genotype Homeodomain Proteins - metabolism Humanities and Social Sciences Immune checkpoint Immunologic Memory Immunological memory Immunotherapy Infections Lymphocytes Lymphocytes T Male Memory cells Mice Mice, Inbred BALB C Mice, Inbred C57BL multidisciplinary NF-AT protein NFATC Transcription Factors - metabolism Receptor mechanisms Receptors Science Science (multidisciplinary) T cell receptors Transcription factors Transcription, Genetic Tumor Escape |
| Title | TOX transcriptionally and epigenetically programs CD8+ T cell exhaustion |
| URI | https://link.springer.com/article/10.1038/s41586-019-1325-x https://www.ncbi.nlm.nih.gov/pubmed/31207603 https://www.proquest.com/docview/2261002818 https://www.proquest.com/docview/2242817827 https://pubmed.ncbi.nlm.nih.gov/PMC6713202 |
| Volume | 571 |
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