Developmental Relationships of Four Exhausted CD8+ T Cell Subsets Reveals Underlying Transcriptional and Epigenetic Landscape Control Mechanisms
CD8+ T cell exhaustion is a major barrier to current anti-cancer immunotherapies. Despite this, the developmental biology of exhausted CD8+ T cells (Tex) remains poorly defined, restraining improvement of strategies aimed at “re-invigorating” Tex cells. Here, we defined a four-cell-stage development...
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| Published in | Immunity (Cambridge, Mass.) Vol. 52; no. 5; pp. 825 - 841.e8 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
19.05.2020
Elsevier Limited |
| Subjects | |
| Online Access | Get full text |
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| Abstract | CD8+ T cell exhaustion is a major barrier to current anti-cancer immunotherapies. Despite this, the developmental biology of exhausted CD8+ T cells (Tex) remains poorly defined, restraining improvement of strategies aimed at “re-invigorating” Tex cells. Here, we defined a four-cell-stage developmental framework for Tex cells. Two TCF1+ progenitor subsets were identified, one tissue restricted and quiescent and one more blood accessible, that gradually lost TCF1 as it divided and converted to a third intermediate Tex subset. This intermediate subset re-engaged some effector biology and increased upon PD-L1 blockade but ultimately converted into a fourth, terminally exhausted subset. By using transcriptional and epigenetic analyses, we identified the control mechanisms underlying subset transitions and defined a key interplay between TCF1, T-bet, and Tox in the process. These data reveal a four-stage developmental hierarchy for Tex cells and define the molecular, transcriptional, and epigenetic mechanisms that could provide opportunities to improve cancer immunotherapy.
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•Ly108 and CD69 define four Tex subsets linked in a hierarchical developmental pathway•Two TCF1+ subsets, effector-like and terminally exhausted subsets, are identified•Key transcriptional, epigenetic, and biological changes define subset transitions•TCF1, T-bet, and Tox coordinate Tex subset development and dynamics
Beltra et al. define a hierarchical developmental pathway for CD8+ T cell exhaustion, revealing four stages and multistep transcriptional and epigenetic dynamics underlying subset transitions and subset-associated biological changes. |
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| AbstractList | CD8+ T cell exhaustion is a major barrier to current anti-cancer immunotherapies. Despite this, the developmental biology of exhausted CD8+ T cells (Tex) remains poorly defined, restraining improvement of strategies aimed at "re-invigorating" Tex cells. Here, we defined a four-cell-stage developmental framework for Tex cells. Two TCF1+ progenitor subsets were identified, one tissue restricted and quiescent and one more blood accessible, that gradually lost TCF1 as it divided and converted to a third intermediate Tex subset. This intermediate subset re-engaged some effector biology and increased upon PD-L1 blockade but ultimately converted into a fourth, terminally exhausted subset. By using transcriptional and epigenetic analyses, we identified the control mechanisms underlying subset transitions and defined a key interplay between TCF1, T-bet, and Tox in the process. These data reveal a four-stage developmental hierarchy for Tex cells and define the molecular, transcriptional, and epigenetic mechanisms that could provide opportunities to improve cancer immunotherapy.CD8+ T cell exhaustion is a major barrier to current anti-cancer immunotherapies. Despite this, the developmental biology of exhausted CD8+ T cells (Tex) remains poorly defined, restraining improvement of strategies aimed at "re-invigorating" Tex cells. Here, we defined a four-cell-stage developmental framework for Tex cells. Two TCF1+ progenitor subsets were identified, one tissue restricted and quiescent and one more blood accessible, that gradually lost TCF1 as it divided and converted to a third intermediate Tex subset. This intermediate subset re-engaged some effector biology and increased upon PD-L1 blockade but ultimately converted into a fourth, terminally exhausted subset. By using transcriptional and epigenetic analyses, we identified the control mechanisms underlying subset transitions and defined a key interplay between TCF1, T-bet, and Tox in the process. These data reveal a four-stage developmental hierarchy for Tex cells and define the molecular, transcriptional, and epigenetic mechanisms that could provide opportunities to improve cancer immunotherapy. CD8+ T cell exhaustion is a major barrier to current anti-cancer immunotherapies. Despite this, the developmental biology of exhausted CD8+ T cells (Tex) remains poorly defined, restraining improvement of strategies aimed at “re-invigorating” Tex cells. Here, we defined a four-cell-stage developmental framework for Tex cells. Two TCF1+ progenitor subsets were identified, one tissue restricted and quiescent and one more blood accessible, that gradually lost TCF1 as it divided and converted to a third intermediate Tex subset. This intermediate subset re-engaged some effector biology and increased upon PD-L1 blockade but ultimately converted into a fourth, terminally exhausted subset. By using transcriptional and epigenetic analyses, we identified the control mechanisms underlying subset transitions and defined a key interplay between TCF1, T-bet, and Tox in the process. These data reveal a four-stage developmental hierarchy for Tex cells and define the molecular, transcriptional, and epigenetic mechanisms that could provide opportunities to improve cancer immunotherapy. [Display omitted] •Ly108 and CD69 define four Tex subsets linked in a hierarchical developmental pathway•Two TCF1+ subsets, effector-like and terminally exhausted subsets, are identified•Key transcriptional, epigenetic, and biological changes define subset transitions•TCF1, T-bet, and Tox coordinate Tex subset development and dynamics Beltra et al. define a hierarchical developmental pathway for CD8+ T cell exhaustion, revealing four stages and multistep transcriptional and epigenetic dynamics underlying subset transitions and subset-associated biological changes. SummaryCD8+ T cell exhaustion is a major barrier to current anti-cancer immunotherapies. Despite this, the developmental biology of exhausted CD8+ T cells (Tex) remains poorly defined, restraining improvement of strategies aimed at “re-invigorating” Tex cells. Here, we defined a four-cell-stage developmental framework for Tex cells. Two TCF1+ progenitor subsets were identified, one tissue restricted and quiescent and one more blood accessible, that gradually lost TCF1 as it divided and converted to a third intermediate Tex subset. This intermediate subset re-engaged some effector biology and increased upon PD-L1 blockade but ultimately converted into a fourth, terminally exhausted subset. By using transcriptional and epigenetic analyses, we identified the control mechanisms underlying subset transitions and defined a key interplay between TCF1, T-bet, and Tox in the process. These data reveal a four-stage developmental hierarchy for Tex cells and define the molecular, transcriptional, and epigenetic mechanisms that could provide opportunities to improve cancer immunotherapy. CD8 + T cell exhaustion is a major barrier to current anti-cancer immunotherapies. Despite this, the developmental biology of exhausted CD8 + T cells (Tex) remains poorly defined, restraining improvement of strategies aimed at “re-invigorating” Tex cells. Here, we defined a four-cell-stage developmental framework for Tex cells. Two TCF1 + progenitor subsets were identified, one tissue restricted and quiescent and one more blood accessible, that gradually lost TCF1 as it divided and converted to a third intermediate Tex subset. This intermediate subset re-engaged some effector biology and increased upon PD-L1 blockade but ultimately converted into a fourth, terminally exhausted subset. By using transcriptional and epigenetic analyses, we identified the control mechanisms underlying subset transitions and defined a key interplay between TCF1, T-bet, and Tox in the process. These data reveal a four-stage developmental hierarchy for Tex cells and define the molecular, transcriptional, and epigenetic mechanisms that could provide opportunities to improve cancer immunotherapy. Beltra et al. define a hierarchical developmental pathway for CD8 + T cell exhaustion, revealing four stages and multistep transcriptional and epigenetic dynamics underlying subset transitions and subset-associated biological changes. CD8 T cell exhaustion is a major barrier to current anti-cancer immunotherapies. Despite this, the developmental biology of exhausted CD8 T cells (Tex) remains poorly defined, restraining improvement of strategies aimed at "re-invigorating" Tex cells. Here, we defined a four-cell-stage developmental framework for Tex cells. Two TCF1 progenitor subsets were identified, one tissue restricted and quiescent and one more blood accessible, that gradually lost TCF1 as it divided and converted to a third intermediate Tex subset. This intermediate subset re-engaged some effector biology and increased upon PD-L1 blockade but ultimately converted into a fourth, terminally exhausted subset. By using transcriptional and epigenetic analyses, we identified the control mechanisms underlying subset transitions and defined a key interplay between TCF1, T-bet, and Tox in the process. These data reveal a four-stage developmental hierarchy for Tex cells and define the molecular, transcriptional, and epigenetic mechanisms that could provide opportunities to improve cancer immunotherapy. |
| Author | Mitchell, Tara C. Abdel-Hakeem, Mohamed S. Khan, Omar Giles, Josephine R. Chen, Zeyu Huang, Yinghui Jane Wherry, E. John Xu, Wei Schuchter, Lynn M. Amaravadi, Ravi K. Huang, Alexander C. Beltra, Jean-Christophe Karakousis, Giorgos C. Ngiow, Shin Foong Nzingha, Kito Casella, Valentina Xu, Xiaowei Yan, Patrick Kurachi, Makoto Manne, Sasikanth |
| AuthorAffiliation | 6 Infection Biology Laboratory, Department of Experimental and Health Sciences (DCEXS), Universitat Pompeu Fabra, Barcelona, Spain 11 Department of Surgery, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA 4 Department of Microbiology and Immunology, Faculty of Pharmacy, Cairo University, Kasr El-Aini, Cairo, Egypt 9 Abramson Cancer Center, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA 12 Lead Contact 1 Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA 7 Arsenal Biosciences, South San Francisco, CA, USA 10 Department of Pathology and Laboratory Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA 5 Department of Molecular Genetics, Graduate School of Medical Sciences, Kanazawa University, Kanazawa, Japan 2 Institute for Immunology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, P |
| AuthorAffiliation_xml | – name: 8 Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA – name: 7 Arsenal Biosciences, South San Francisco, CA, USA – name: 12 Lead Contact – name: 6 Infection Biology Laboratory, Department of Experimental and Health Sciences (DCEXS), Universitat Pompeu Fabra, Barcelona, Spain – name: 4 Department of Microbiology and Immunology, Faculty of Pharmacy, Cairo University, Kasr El-Aini, Cairo, Egypt – name: 3 Parker Institute for Cancer Immunotherapy at University of Pennsylvania, Philadelphia, PA, USA – name: 9 Abramson Cancer Center, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA – name: 5 Department of Molecular Genetics, Graduate School of Medical Sciences, Kanazawa University, Kanazawa, Japan – name: 11 Department of Surgery, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA – name: 10 Department of Pathology and Laboratory Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA – name: 2 Institute for Immunology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 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: Jean-Christophe surname: Beltra fullname: Beltra, Jean-Christophe organization: Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA – sequence: 2 givenname: Sasikanth surname: Manne fullname: Manne, Sasikanth organization: Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA – sequence: 3 givenname: Mohamed S. surname: Abdel-Hakeem fullname: Abdel-Hakeem, Mohamed S. organization: Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA – sequence: 4 givenname: Makoto surname: Kurachi fullname: Kurachi, Makoto organization: Department of Molecular Genetics, Graduate School of Medical Sciences, Kanazawa University, Kanazawa, Japan – sequence: 5 givenname: Josephine R. surname: Giles fullname: Giles, Josephine R. organization: Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA – sequence: 6 givenname: Zeyu surname: Chen fullname: Chen, Zeyu organization: Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA – sequence: 7 givenname: Valentina surname: Casella fullname: Casella, Valentina organization: Infection Biology Laboratory, Department of Experimental and Health Sciences (DCEXS), Universitat Pompeu Fabra, Barcelona, Spain – sequence: 8 givenname: Shin Foong surname: Ngiow fullname: Ngiow, Shin Foong organization: Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA – sequence: 9 givenname: Omar surname: Khan fullname: Khan, Omar organization: Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA – sequence: 10 givenname: Yinghui Jane surname: Huang fullname: Huang, Yinghui Jane organization: Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA – sequence: 11 givenname: Patrick surname: Yan fullname: Yan, Patrick organization: Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA – sequence: 12 givenname: Kito surname: Nzingha fullname: Nzingha, Kito organization: Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA – sequence: 13 givenname: Wei surname: Xu fullname: Xu, Wei organization: Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA – sequence: 14 givenname: Ravi K. surname: Amaravadi fullname: Amaravadi, Ravi K. organization: Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA – sequence: 15 givenname: Xiaowei surname: Xu fullname: Xu, Xiaowei organization: Abramson Cancer Center, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA – sequence: 16 givenname: Giorgos C. surname: Karakousis fullname: Karakousis, Giorgos C. organization: Abramson Cancer Center, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA – sequence: 17 givenname: Tara C. surname: Mitchell fullname: Mitchell, Tara C. organization: Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA – sequence: 18 givenname: Lynn M. surname: Schuchter fullname: Schuchter, Lynn M. organization: Department of Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA – sequence: 19 givenname: Alexander C. surname: Huang fullname: Huang, Alexander C. organization: Institute for Immunology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA – sequence: 20 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, Philadelphia, PA, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32396847$$D View this record in MEDLINE/PubMed |
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| Keywords | T cell exhaustion lineage chronic infection CD8 cancer immunotherapy exhaustion PD-1 blockade Tox TCF1 T-bet epigenetics |
| Language | English |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 AUTHOR CONTRIBUTIONS J.-C.B. and E.J.W. designed the experiments. J.-C.B. performed and analyzed the experiments with help from M.A.-H., V.C., and K.N. J.G. processed the ATAC-seq data. S.M. and J.-C.B. analyzed RNA-seq and ATAC-seq data. M.K., J.-C.B., S.F.N., and O.K. produced RV. Z.C. and Y.J.H. developed Tcf7cKO and Tox+/− mice. P.Y. and A.C.H. analyzed human samples. W.X., R.K.A., X.X., G.C.K., T.C.M., and L.M.S. coordinated human sample collection. J.-C.B. and E.J.W. wrote the manuscript. |
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| Snippet | CD8+ T cell exhaustion is a major barrier to current anti-cancer immunotherapies. Despite this, the developmental biology of exhausted CD8+ T cells (Tex)... CD8 T cell exhaustion is a major barrier to current anti-cancer immunotherapies. Despite this, the developmental biology of exhausted CD8 T cells (Tex) remains... SummaryCD8+ T cell exhaustion is a major barrier to current anti-cancer immunotherapies. Despite this, the developmental biology of exhausted CD8+ T cells... CD8+ T cell exhaustion is a major barrier to current anti-cancer immunotherapies. Despite this, the developmental biology of exhausted CD8+ T cells (Tex)... CD8 + T cell exhaustion is a major barrier to current anti-cancer immunotherapies. Despite this, the developmental biology of exhausted CD8 + T cells (Tex)... |
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| SubjectTerms | Animals B7-H1 Antigen - genetics B7-H1 Antigen - immunology Biological effects Biology Cancer Cancer immunotherapy CD8 CD8 antigen CD8-Positive T-Lymphocytes - cytology CD8-Positive T-Lymphocytes - immunology CD8-Positive T-Lymphocytes - metabolism Cell cycle Cells, Cultured chronic infection Developmental biology Epigenesis, Genetic - genetics Epigenesis, Genetic - immunology Epigenetics Exhaustion Hepatocyte nuclear factor 1 Hepatocyte Nuclear Factor 1-alpha - genetics Hepatocyte Nuclear Factor 1-alpha - immunology Homeodomain Proteins - genetics Homeodomain Proteins - immunology Humans Immunotherapy Immunotherapy - methods Infections Lymphocytes Lymphocytes T Mice, Inbred C57BL Neoplasms - genetics Neoplasms - immunology Neoplasms - therapy PD-1 blockade PD-L1 protein Population T cell exhaustion lineage T cell receptors T-bet T-Box Domain Proteins - genetics T-Box Domain Proteins - immunology T-Lymphocyte Subsets - immunology T-Lymphocyte Subsets - metabolism TCF1 Tox Transcription Transcription, Genetic - genetics Transcription, Genetic - immunology Tumors Viral infections |
| Title | Developmental Relationships of Four Exhausted CD8+ T Cell Subsets Reveals Underlying Transcriptional and Epigenetic Landscape Control Mechanisms |
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