Cancer-Germline Antigen Expression Discriminates Clinical Outcome to CTLA-4 Blockade
CTLA-4 immune checkpoint blockade is clinically effective in a subset of patients with metastatic melanoma. We identify a subcluster of MAGE-A cancer-germline antigens, located within a narrow 75 kb region of chromosome Xq28, that predicts resistance uniquely to blockade of CTLA-4, but not PD-1. We...
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| Published in | Cell Vol. 173; no. 3; pp. 624 - 633.e8 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
19.04.2018
|
| Subjects | |
| Online Access | Get full text |
| ISSN | 0092-8674 1097-4172 1097-4172 |
| DOI | 10.1016/j.cell.2018.03.026 |
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| Abstract | CTLA-4 immune checkpoint blockade is clinically effective in a subset of patients with metastatic melanoma. We identify a subcluster of MAGE-A cancer-germline antigens, located within a narrow 75 kb region of chromosome Xq28, that predicts resistance uniquely to blockade of CTLA-4, but not PD-1. We validate this gene expression signature in an independent anti-CTLA-4-treated cohort and show its specificity to the CTLA-4 pathway with two independent anti-PD-1-treated cohorts. Autophagy, a process critical for optimal anti-cancer immunity, has previously been shown to be suppressed by the MAGE-TRIM28 ubiquitin ligase in vitro. We now show that the expression of the key autophagosome component LC3B and other activators of autophagy are negatively associated with MAGE-A protein levels in human melanomas, including samples from patients with resistance to CTLA-4 blockade. Our findings implicate autophagy suppression in resistance to CTLA-4 blockade in melanoma, suggesting exploitation of autophagy induction for potential therapeutic synergy with CTLA-4 inhibitors.
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•Increased expression of a MAGE-A subcluster predicts resistance to CTLA-4 blockade•This MAGE-A subcluster marks a distinct, epigenetically defined subset of melanomas•This gene signature is specific to resistance to CTLA-4, but not PD-1, blockade•Autophagy is implicated in clinical resistance to CTLA-4 blockade
Increased expression of a subcluster of MAGE-A cancer-germline antigens predicts resistance specific to CTLA-4, but not PD-1, blockade, and its association with autophagy suppression implicates the role of autophagy in regulating primary resistance to anti-CTLA-4 therapy in melanoma patients. |
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| AbstractList | CTLA-4 immune checkpoint blockade is clinically effective in a subset of patients with metastatic melanoma. We identify a subcluster of MAGE-A cancer-germline antigens, located within a narrow 75 kb region of chromosome Xq28, that predicts resistance uniquely to blockade of CTLA-4, but not PD-1. We validate this gene expression signature in an independent anti-CTLA-4-treated cohort and show its specificity to the CTLA-4 pathway with two independent anti-PD-1-treated cohorts. Autophagy, a process critical for optimal anti-cancer immunity, has previously been shown to be suppressed by the MAGE-TRIM28 ubiquitin ligase in vitro. We now show that the expression of the key autophagosome component LC3B and other activators of autophagy are negatively associated with MAGE-A protein levels in human melanomas, including samples from patients with resistance to CTLA-4 blockade. Our findings implicate autophagy suppression in resistance to CTLA-4 blockade in melanoma, suggesting exploitation of autophagy induction for potential therapeutic synergy with CTLA-4 inhibitors.
[Display omitted]
•Increased expression of a MAGE-A subcluster predicts resistance to CTLA-4 blockade•This MAGE-A subcluster marks a distinct, epigenetically defined subset of melanomas•This gene signature is specific to resistance to CTLA-4, but not PD-1, blockade•Autophagy is implicated in clinical resistance to CTLA-4 blockade
Increased expression of a subcluster of MAGE-A cancer-germline antigens predicts resistance specific to CTLA-4, but not PD-1, blockade, and its association with autophagy suppression implicates the role of autophagy in regulating primary resistance to anti-CTLA-4 therapy in melanoma patients. CTLA-4 immune checkpoint blockade is clinically effective in a subset of patients with metastatic melanoma. We identify a subcluster of MAGE-A cancer-germline antigens, located within a narrow 75 kb region of chromosome Xq28, that predicts resistance uniquely to blockade of CTLA-4, but not PD-1. We validate this gene expression signature in an independent anti-CTLA-4-treated cohort and show its specificity to the CTLA-4 pathway with two independent anti-PD-1-treated cohorts. Autophagy, a process critical for optimal anti-cancer immunity, has previously been shown to be suppressed by the MAGE-TRIM28 ubiquitin ligase in vitro. We now show that the expression of the key autophagosome component LC3B and other activators of autophagy are negatively associated with MAGE-A protein levels in human melanomas, including samples from patients with resistance to CTLA-4 blockade. Our findings implicate autophagy suppression in resistance to CTLA-4 blockade in melanoma, suggesting exploitation of autophagy induction for potential therapeutic synergy with CTLA-4 inhibitors.CTLA-4 immune checkpoint blockade is clinically effective in a subset of patients with metastatic melanoma. We identify a subcluster of MAGE-A cancer-germline antigens, located within a narrow 75 kb region of chromosome Xq28, that predicts resistance uniquely to blockade of CTLA-4, but not PD-1. We validate this gene expression signature in an independent anti-CTLA-4-treated cohort and show its specificity to the CTLA-4 pathway with two independent anti-PD-1-treated cohorts. Autophagy, a process critical for optimal anti-cancer immunity, has previously been shown to be suppressed by the MAGE-TRIM28 ubiquitin ligase in vitro. We now show that the expression of the key autophagosome component LC3B and other activators of autophagy are negatively associated with MAGE-A protein levels in human melanomas, including samples from patients with resistance to CTLA-4 blockade. Our findings implicate autophagy suppression in resistance to CTLA-4 blockade in melanoma, suggesting exploitation of autophagy induction for potential therapeutic synergy with CTLA-4 inhibitors. CTLA-4 immune checkpoint blockade is clinically effective in a subset of patients with metastatic melanoma. We identify a subcluster of MAGE-A cancer-germline antigens, located within a narrow 75 kb region of chromosome Xq28, that predicts resistance uniquely to blockade of CTLA-4, but not PD-1. We validate this gene expression signature in an independent anti-CTLA-4-treated cohort and show its specificity to the CTLA-4 pathway with two independent anti-PD-1-treated cohorts. Autophagy, a process critical for optimal anti-cancer immunity, has previously been shown to be suppressed by the MAGE-TRIM28 ubiquitin ligase in vitro. We now show that the expression of the key autophagosome component LC3B and other activators of autophagy are negatively associated with MAGE-A protein levels in human melanomas, including samples from patients with resistance to CTLA-4 blockade. Our findings implicate autophagy suppression in resistance to CTLA-4 blockade in melanoma, suggesting exploitation of autophagy induction for potential therapeutic synergy with CTLA-4 inhibitors. CTLA-4 immune checkpoint blockade is clinically effective in a subset of patients with metastatic melanoma. We identify a subcluster of MAGE-A cancer-germline antigens, located within a narrow 75 kb region of chromosome Xq28, that predicts resistance uniquely to blockade of CTLA-4, but not PD-1. We validate this gene expression signature in an independent anti-CTLA-4-treated cohort and show its specificity to the CTLA-4 pathway with two independent anti-PD-1-treated cohorts. Autophagy, a process critical for optimal anti-cancer immunity, has been previously shown to be suppressed by the MAGE-TRIM28 ubiquitin ligase in vitro . We now show that the expression of the key autophagosome component LC3B and other activators of autophagy are negatively associated with MAGE-A protein levels in human melanomas, including samples from patients with resistance to CTLA-4 blockade. Our findings implicate autophagy suppression in resistance to CTLA-4 blockade in melanoma, suggesting exploitation of autophagy induction for potential therapeutic synergy with CTLA-4 inhibitors. Increased expression of a subcluster of MAGE-A cancer-germline antigens predicts resistance specific to CTLA4, but not PD1, blockade, and its association with autophagy suppression implicates the role autophagy in regulating primary resistance to anti-CTLA4 therapy in melanoma patients CTLA-4 immune checkpoint blockade is clinically effective in a subset of patients with metastatic melanoma. We identify a subcluster of MAGE-A cancer-germline antigens, located within a narrow 75 kb region of chromosome Xq28, that predicts resistance uniquely to blockade of CTLA-4, but not PD-1. We validate this gene expression signature in an independent anti-CTLA-4-treated cohort and show its specificity to the CTLA-4 pathway with two independent anti-PD-1-treated cohorts. Autophagy, a process critical for optimal anti-cancer immunity, has previously been shown to be suppressed by the MAGE-TRIM28 ubiquitin ligase in vitro. We now show that the expression of the key autophagosome component LC3B and other activators of autophagy are negatively associated with MAGE-A protein levels in human melanomas, including samples from patients with resistance to CTLA-4 blockade. Our findings implicate autophagy suppression in resistance to CTLA-4 blockade in melanoma, suggesting exploitation of autophagy induction for potential therapeutic synergy with CTLA-4 inhibitors. |
| Author | Cartun, Zachary J. Neuberg, Donna Mohammad, Arman Gnirke, Andreas Meissner, Alexander Hodi, F. Stephen Zhan, Qian Keskin, Derin B. Bachireddy, Pavan Murphy, George F. Gusenleitner, Daniel Galonska, Christina Bango, Clyde Lee, Patrick C. Huang, Ying Shukla, Sachet A. Schadendorf, Dirk Langer, Rupert Weber, Jeffrey S. Van Allen, Eliezer M. Hacohen, Nir Miao, Diana Snyder, Alexandra Schilling, Bastian Merghoub, Taha Wu, Catherine J. Wolchok, Jedd D. Babadi, Mehrtash Lian, Christine G. Garraway, Levi A. Potts, Patrick R. Clement, Kendell |
| AuthorAffiliation | 14 Department of Pathology, University of Bern, 3012 Bern, Switzerland 5 Department of Dermatology, Venereology and Allergology, University Hospital Würzburg, 97080 Würzburg, Germany 1 Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02215, USA 8 Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, Massachusetts 02138, USA 10 Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY USA 11 New York University Langone Medical Center, New York, NY 10016, USA 12 Department of Biostatistics and Computational Biology, Dana-Farber Cancer Institute, Boston, Massachusetts 02115, USA 9 Weill Cornell Medical College, New York, NY, USA 2 Broad Institute, Cambridge, MA 02142, USA 4 Department of Dermatology, University Hospital, University Duisburg—Essen, 45147 Essen, Germany and German Cancer Consortium (DKTK), 69121 Heidelberg, Germany 3 Department of Medicine, Brigham & Women’s Hospital, Boston, MA 02115, USA 6 |
| AuthorAffiliation_xml | – name: 3 Department of Medicine, Brigham & Women’s Hospital, Boston, MA 02115, USA – name: 13 Department of Cell and Molecular Biology, St. Jude Children’s Research Hospital, Memphis, TN 38105-3678, USA – name: 11 New York University Langone Medical Center, New York, NY 10016, USA – name: 6 Max Planck Institute for Molecular Genetics, 14195 Berlin, Germany – name: 14 Department of Pathology, University of Bern, 3012 Bern, Switzerland – name: 12 Department of Biostatistics and Computational Biology, Dana-Farber Cancer Institute, Boston, Massachusetts 02115, USA – name: 1 Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02215, USA – name: 9 Weill Cornell Medical College, New York, NY, USA – name: 7 Program in Dermatopathology, Department of Pathology, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA – name: 2 Broad Institute, Cambridge, MA 02142, USA – name: 4 Department of Dermatology, University Hospital, University Duisburg—Essen, 45147 Essen, Germany and German Cancer Consortium (DKTK), 69121 Heidelberg, Germany – name: 10 Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY USA – name: 5 Department of Dermatology, Venereology and Allergology, University Hospital Würzburg, 97080 Würzburg, Germany – name: 8 Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, Massachusetts 02138, USA |
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fullname: Lian, Christine G. organization: Program in Dermatopathology, Department of Pathology, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA – sequence: 30 givenname: Dirk surname: Schadendorf fullname: Schadendorf, Dirk organization: Department of Dermatology, University Hospital, University Duisburg-Essen, 45147 Essen, Germany – sequence: 31 givenname: F. 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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29656892$$D View this record in MEDLINE/PubMed |
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| Issue | 3 |
| Keywords | immunogenomics checkpoint blockade cancer-germline antigen autophagy ipilimumab immunotherapy melanoma CTLA-4 MAGE-A PD-1 |
| Language | English |
| License | This article is made available under the Elsevier license. Copyright © 2018 Elsevier Inc. All rights reserved. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 These authors contributed equally |
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| SubjectTerms | Animals Antibodies, Monoclonal - therapeutic use antigens Antigens, Neoplasm - genetics Antigens, Neoplasm - immunology Autophagy cancer-germline antigen Cell Line, Tumor checkpoint blockade chromosomes CTLA-4 CTLA-4 Antigen - genetics CTLA-4 Antigen - immunology DNA Methylation Epigenesis, Genetic Female gene expression Gene Expression Profiling Germ-Line Mutation Humans immunogenomics Immunotherapy ipilimumab Ipilimumab - pharmacology MAGE-A Male melanoma Melanoma - genetics Melanoma - immunology Melanoma-Specific Antigens - genetics Melanoma-Specific Antigens - immunology metastasis Mice Mice, Transgenic Neoplasms - genetics Neoplasms - immunology patients PD-1 protein content Skin Neoplasms - genetics Skin Neoplasms - immunology therapeutics ubiquitin-protein ligase |
| Title | Cancer-Germline Antigen Expression Discriminates Clinical Outcome to CTLA-4 Blockade |
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