Cholesterol Induces CD8+ T Cell Exhaustion in the Tumor Microenvironment
Tumor-infiltrating T cells often lose their effector function; however, the mechanisms are incompletely understood. We report that cholesterol in the tumor microenvironment induces CD8+ T cell expression of immune checkpoints and exhaustion. Tumor tissues enriched with cholesterol and cholesterol co...
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| Published in | Cell metabolism Vol. 30; no. 1; pp. 143 - 156.e5 |
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| Main Authors | , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
02.07.2019
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Tumor-infiltrating T cells often lose their effector function; however, the mechanisms are incompletely understood. We report that cholesterol in the tumor microenvironment induces CD8+ T cell expression of immune checkpoints and exhaustion. Tumor tissues enriched with cholesterol and cholesterol content in tumor-infiltrating CD8+ T cells were positively and progressively associated with upregulated T cell expression of PD-1, 2B4, TIM-3, and LAG-3. Adoptively transferred CD8+ T cells acquired cholesterol, expressed high levels of immune checkpoints, and became exhausted upon entering a tumor. Tumor culture supernatant or cholesterol induced immune checkpoint expression by increasing endoplasmic reticulum (ER) stress in CD8+ T cells. Consequently, the ER stress sensor XBP1 was activated and regulated PD-1 and 2B4 transcription. Inhibiting XBP1 or reducing cholesterol in CD8+ T cells effectively restored antitumor activity. This study reveals a mechanism underlying T cell exhaustion and suggests a new strategy for restoring T cell function by reducing cholesterol to enhance T cell-based immunotherapy.
[Display omitted]
•CD8+ T cell exhaustion is correlated with a high cholesterol level•Tumor microenvironment is enriched with cholesterol•Cholesterol in the tumor microenvironment induces CD8+ T cell exhaustion•ER stress-XBP1 pathway is required for cholesterol-induced CD8+ T cell exhaustion
Tumor-infiltrating T cells often lose their effector function. Ma et al. show that cholesterol in the tumor microenvironment induces CD8+ T cell exhaustion in an ER-stress-XBP1-dependent manner. Reducing cholesterol or ER stress enhanced CD8+ T cell antitumor function, highlighting therapeutic avenues to improve T cell-based immunotherapy in the clinic. |
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| AbstractList | Tumor-infiltrating T cells often lose their effector function; however, the mechanisms are incompletely understood. We report that cholesterol in the tumor microenvironment induces CD8
T cell expression of immune checkpoints and exhaustion. Tumor tissues enriched with cholesterol and cholesterol content in tumor-infiltrating CD8
T cells were positively and progressively associated with upregulated T cell expression of PD-1, 2B4, TIM-3, and LAG-3. Adoptively transferred CD8
T cells acquired cholesterol, expressed high levels of immune checkpoints, and became exhausted upon entering a tumor. Tumor culture supernatant or cholesterol induced immune checkpoint expression by increasing endoplasmic reticulum (ER) stress in CD8
T cells. Consequently, the ER stress sensor XBP1 was activated and regulated PD-1 and 2B4 transcription. Inhibiting XBP1 or reducing cholesterol in CD8
T cells effectively restored antitumor activity. This study reveals a mechanism underlying T cell exhaustion and suggests a new strategy for restoring T cell function by reducing cholesterol to enhance T cell-based immunotherapy. Tumor-infiltrating T cells often lose their effector function; however, the mechanisms are incompletely understood. We report that cholesterol in the tumor microenvironment induces CD8+ T cell expression of immune checkpoints and exhaustion. Tumor tissues enriched with cholesterol and cholesterol content in tumor-infiltrating CD8+ T cells were positively and progressively associated with upregulated T cell expression of PD-1, 2B4, TIM-3, and LAG-3. Adoptively transferred CD8+ T cells acquired cholesterol, expressed high levels of immune checkpoints, and became exhausted upon entering a tumor. Tumor culture supernatant or cholesterol induced immune checkpoint expression by increasing endoplasmic reticulum (ER) stress in CD8+ T cells. Consequently, the ER stress sensor XBP1 was activated and regulated PD-1 and 2B4 transcription. Inhibiting XBP1 or reducing cholesterol in CD8+ T cells effectively restored antitumor activity. This study reveals a mechanism underlying T cell exhaustion and suggests a new strategy for restoring T cell function by reducing cholesterol to enhance T cell-based immunotherapy. [Display omitted] •CD8+ T cell exhaustion is correlated with a high cholesterol level•Tumor microenvironment is enriched with cholesterol•Cholesterol in the tumor microenvironment induces CD8+ T cell exhaustion•ER stress-XBP1 pathway is required for cholesterol-induced CD8+ T cell exhaustion Tumor-infiltrating T cells often lose their effector function. Ma et al. show that cholesterol in the tumor microenvironment induces CD8+ T cell exhaustion in an ER-stress-XBP1-dependent manner. Reducing cholesterol or ER stress enhanced CD8+ T cell antitumor function, highlighting therapeutic avenues to improve T cell-based immunotherapy in the clinic. Tumor-infiltrating T cells often lose their effector function; however, the mechanisms are incompletely understood. We report that cholesterol in the tumor microenvironment induces CD8 + T-cell expression of immune checkpoints and exhaustion. Tumor tissues enriched with cholesterol and cholesterol content in tumor-infiltrating CD8 + T cells was positively and progressively associated with upregulated T-cell expression of PD-1, 2B4, TIM-3, and LAG-3. Adoptively transferred CD8 + T cells acquired cholesterol, expressed high levels of immune checkpoints, and became exhausted upon entering tumor. Tumor-culture supernatant or cholesterol induced immune checkpoint expression by increasing endoplasmic reticulum (ER) stress in CD8 + T cells. Consequently, the ER-stress sensor XBP1 was activated and regulated PD-1 and 2B4 transcription. Inhibiting XBP1 or reducing cholesterol in CD8 + T cells effectively restored antitumor activity. This study reveals a novel mechanism underlying T cell exhaustion and suggests a new strategy for restoring T cell function by reducing cholesterol to enhance T-cell based immunotherapy. Tumor-infiltrating T cells often lose their effector function. Ma et al. show that cholesterol in the tumor microenvironment induces CD8 + T-cell exhaustion in an ER-stress-XBP1 dependent manner. Reducing cholesterol or ER stress enhanced CD8 + T-cell anti-tumor function, highlighting therapeutic avenues to improve T-cell based immunotherapy in the clinic. Tumor-infiltrating T cells often lose their effector function; however, the mechanisms are incompletely understood. We report that cholesterol in the tumor microenvironment induces CD8+ T cell expression of immune checkpoints and exhaustion. Tumor tissues enriched with cholesterol and cholesterol content in tumor-infiltrating CD8+ T cells were positively and progressively associated with upregulated T cell expression of PD-1, 2B4, TIM-3, and LAG-3. Adoptively transferred CD8+ T cells acquired cholesterol, expressed high levels of immune checkpoints, and became exhausted upon entering a tumor. Tumor culture supernatant or cholesterol induced immune checkpoint expression by increasing endoplasmic reticulum (ER) stress in CD8+ T cells. Consequently, the ER stress sensor XBP1 was activated and regulated PD-1 and 2B4 transcription. Inhibiting XBP1 or reducing cholesterol in CD8+ T cells effectively restored antitumor activity. This study reveals a mechanism underlying T cell exhaustion and suggests a new strategy for restoring T cell function by reducing cholesterol to enhance T cell-based immunotherapy.Tumor-infiltrating T cells often lose their effector function; however, the mechanisms are incompletely understood. We report that cholesterol in the tumor microenvironment induces CD8+ T cell expression of immune checkpoints and exhaustion. Tumor tissues enriched with cholesterol and cholesterol content in tumor-infiltrating CD8+ T cells were positively and progressively associated with upregulated T cell expression of PD-1, 2B4, TIM-3, and LAG-3. Adoptively transferred CD8+ T cells acquired cholesterol, expressed high levels of immune checkpoints, and became exhausted upon entering a tumor. Tumor culture supernatant or cholesterol induced immune checkpoint expression by increasing endoplasmic reticulum (ER) stress in CD8+ T cells. Consequently, the ER stress sensor XBP1 was activated and regulated PD-1 and 2B4 transcription. Inhibiting XBP1 or reducing cholesterol in CD8+ T cells effectively restored antitumor activity. This study reveals a mechanism underlying T cell exhaustion and suggests a new strategy for restoring T cell function by reducing cholesterol to enhance T cell-based immunotherapy. |
| Author | Yi, Qing Kalady, Matthew F. Wang, Qiang Bi, Enguang Yang, Maojie Su, Pan Liu, Lintao Qian, Jianfei Ma, Xingzhe Huang, Chunjian Lu, Yong Zhang, Aijun Zheng, Chengyun Hamilton, Dale J. Gupte, Anisha A. |
| AuthorAffiliation | 1 Center for Translational Research in Hematologic Malignancies, Houston Methodist Cancer Center/Houston Methodist Research Institute, Houston Methodist, Houston, TX 77030, USA 5 Department of Hematology, Second Hospital of Shandong University, Jinan 250033, China 2 Department of Microbiology & Immunology, Wake Forest School of Medicine, Winston-Salem, North Carolina 27109, USA 4 Center for Bioenergetics, Houston Methodist Research Institute, Houston, TX 77030, USA 6 Lead Contact 3 Department of Colorectal Surgery, Digestive Disease Institute, Cleveland Clinic, Cleveland, Ohio 44195, USA |
| AuthorAffiliation_xml | – name: 5 Department of Hematology, Second Hospital of Shandong University, Jinan 250033, China – name: 6 Lead Contact – name: 2 Department of Microbiology & Immunology, Wake Forest School of Medicine, Winston-Salem, North Carolina 27109, USA – name: 4 Center for Bioenergetics, Houston Methodist Research Institute, Houston, TX 77030, USA – name: 3 Department of Colorectal Surgery, Digestive Disease Institute, Cleveland Clinic, Cleveland, Ohio 44195, USA – name: 1 Center for Translational Research in Hematologic Malignancies, Houston Methodist Cancer Center/Houston Methodist Research Institute, Houston Methodist, Houston, TX 77030, USA |
| Author_xml | – sequence: 1 givenname: Xingzhe surname: Ma fullname: Ma, Xingzhe organization: Center for Translational Research in Hematologic Malignancies, Houston Methodist Cancer Center, Houston Methodist Research Institute, Houston, TX 77030, USA – sequence: 2 givenname: Enguang surname: Bi fullname: Bi, Enguang organization: Center for Translational Research in Hematologic Malignancies, Houston Methodist Cancer Center, Houston Methodist Research Institute, Houston, TX 77030, USA – sequence: 3 givenname: Yong surname: Lu fullname: Lu, Yong organization: Department of Microbiology & Immunology, Wake Forest School of Medicine, Winston-Salem, NC 27109, USA – sequence: 4 givenname: Pan surname: Su fullname: Su, Pan organization: Center for Translational Research in Hematologic Malignancies, Houston Methodist Cancer Center, Houston Methodist Research Institute, Houston, TX 77030, USA – sequence: 5 givenname: Chunjian surname: Huang fullname: Huang, Chunjian organization: Center for Translational Research in Hematologic Malignancies, Houston Methodist Cancer Center, Houston Methodist Research Institute, Houston, TX 77030, USA – sequence: 6 givenname: Lintao surname: Liu fullname: Liu, Lintao organization: Center for Translational Research in Hematologic Malignancies, Houston Methodist Cancer Center, Houston Methodist Research Institute, Houston, TX 77030, USA – sequence: 7 givenname: Qiang surname: Wang fullname: Wang, Qiang organization: Center for Translational Research in Hematologic Malignancies, Houston Methodist Cancer Center, Houston Methodist Research Institute, Houston, TX 77030, USA – sequence: 8 givenname: Maojie surname: Yang fullname: Yang, Maojie organization: Center for Translational Research in Hematologic Malignancies, Houston Methodist Cancer Center, Houston Methodist Research Institute, Houston, TX 77030, USA – sequence: 9 givenname: Matthew F. surname: Kalady fullname: Kalady, Matthew F. organization: Department of Colorectal Surgery, Digestive Disease Institute, Cleveland Clinic, Cleveland, OH 44195, USA – sequence: 10 givenname: Jianfei surname: Qian fullname: Qian, Jianfei organization: Center for Translational Research in Hematologic Malignancies, Houston Methodist Cancer Center, Houston Methodist Research Institute, Houston, TX 77030, USA – sequence: 11 givenname: Aijun surname: Zhang fullname: Zhang, Aijun organization: Center for Bioenergetics, Houston Methodist Research Institute, Houston, TX 77030, USA – sequence: 12 givenname: Anisha A. surname: Gupte fullname: Gupte, Anisha A. organization: Center for Bioenergetics, Houston Methodist Research Institute, Houston, TX 77030, USA – sequence: 13 givenname: Dale J. surname: Hamilton fullname: Hamilton, Dale J. organization: Center for Bioenergetics, Houston Methodist Research Institute, Houston, TX 77030, USA – sequence: 14 givenname: Chengyun surname: Zheng fullname: Zheng, Chengyun organization: Department of Hematology, Second Hospital of Shandong University, Jinan 250033, China – sequence: 15 givenname: Qing surname: Yi fullname: Yi, Qing email: qyi@houstonmethodist.org organization: Center for Translational Research in Hematologic Malignancies, Houston Methodist Cancer Center, Houston Methodist Research Institute, Houston, TX 77030, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31031094$$D View this record in MEDLINE/PubMed |
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| Copyright | 2019 Elsevier Inc. Copyright © 2019 Elsevier Inc. All rights reserved. |
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| IngestDate | Thu Aug 21 14:35:03 EDT 2025 Fri Jul 11 06:50:25 EDT 2025 Thu Apr 03 06:56:28 EDT 2025 Tue Jul 01 03:58:18 EDT 2025 Thu Apr 24 22:58:19 EDT 2025 Fri Aug 02 08:58:28 EDT 2024 |
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| Issue | 1 |
| Keywords | exhaustion CD8+ T cells cholesterol tumor microenvironment immune checkpoints |
| Language | English |
| License | Copyright © 2019 Elsevier Inc. All rights reserved. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 AUTHOR CONTRIBUTIONS These authors contributed equally to this work. Q.Y. and X.M initiated the study, designed the experiments, and wrote the paper; X.M. performed most of the experiments and statistical analyses; E.B. edited the paper and provided critical suggestions. Y.L., P.S., C.H., L.L., Q.W., M.Y., M.F. K., J.Q. and C.Z. provided important suggestions or patient samples. A.Z., A.G., D.H. helped with Seahorse Assay. |
| OpenAccessLink | http://www.cell.com/article/S155041311930186X/pdf |
| PMID | 31031094 |
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| PublicationTitle | Cell metabolism |
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| Snippet | Tumor-infiltrating T cells often lose their effector function; however, the mechanisms are incompletely understood. We report that cholesterol in the tumor... Tumor-infiltrating T cells often lose their effector function; however, the mechanisms are incompletely understood. We report that cholesterol in the tumor... |
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| SubjectTerms | CD8+ T cells cholesterol exhaustion immune checkpoints tumor microenvironment |
| Title | Cholesterol Induces CD8+ T Cell Exhaustion in the Tumor Microenvironment |
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