Genomic and Single-Cell Landscape Reveals Novel Drivers and Therapeutic Vulnerabilities of Transformed Cutaneous T-cell Lymphoma
Cutaneous T-cell lymphoma (CTCL) is a rare cancer of skin-homing T cells. A subgroup of patients develops large cell transformation with rapid progression to an aggressive lymphoma. Here, we investigated the transformed CTCL (tCTCL) tumor ecosystem using integrative multiomics spanning whole-exome s...
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| Published in | Cancer discovery Vol. 12; no. 5; pp. 1294 - 1313 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
02.05.2022
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| Subjects | |
| Online Access | Get full text |
| ISSN | 2159-8274 2159-8290 2159-8290 |
| DOI | 10.1158/2159-8290.CD-21-1207 |
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| Abstract | Cutaneous T-cell lymphoma (CTCL) is a rare cancer of skin-homing T cells. A subgroup of patients develops large cell transformation with rapid progression to an aggressive lymphoma. Here, we investigated the transformed CTCL (tCTCL) tumor ecosystem using integrative multiomics spanning whole-exome sequencing (WES), single-cell RNA sequencing, and immune profiling in a unique cohort of 56 patients. WES of 70 skin biopsies showed high tumor mutation burden, UV signatures that are prognostic for survival, exome-based driver events, and most recurrently mutated pathways in tCTCL. Single-cell profiling of 16 tCTCL skin biopsies identified a core oncogenic program with metabolic reprogramming toward oxidative phosphorylation (OXPHOS), cellular plasticity, upregulation of MYC and E2F activities, and downregulation of MHC I suggestive of immune escape. Pharmacologic perturbation using OXPHOS and MYC inhibitors demonstrated potent antitumor activities, whereas immune profiling provided in situ evidence of intercellular communications between malignant T cells expressing macrophage migration inhibitory factor and macrophages and B cells expressing CD74.
Our study contributes a key resource to the community with the largest collection of tCTCL biopsies that are difficult to obtain. The multiomics data herein provide the first comprehensive compendium of genomic alterations in tCTCL and identify potential prognostic signatures and novel therapeutic targets for an incurable T-cell lymphoma. This article is highlighted in the In This Issue feature, p. 1171. |
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| AbstractList | Cutaneous T-cell lymphoma (CTCL) is a rare cancer of skin-homing T cells. A subgroup of patients develops large cell transformation with rapid progression to an aggressive lymphoma. Here, we investigated the transformed CTCL (tCTCL) tumor ecosystem using integrative multiomics spanning whole-exome sequencing (WES), single-cell RNA sequencing, and immune profiling in a unique cohort of 56 patients. WES of 70 skin biopsies showed high tumor mutation burden, UV signatures that are prognostic for survival, exome-based driver events, and most recurrently mutated pathways in tCTCL. Single-cell profiling of 16 tCTCL skin biopsies identified a core oncogenic program with metabolic reprogramming toward oxidative phosphorylation (OXPHOS), cellular plasticity, upregulation of MYC and E2F activities, and downregulation of MHC I suggestive of immune escape. Pharmacologic perturbation using OXPHOS and MYC inhibitors demonstrated potent antitumor activities, whereas immune profiling provided in situ evidence of intercellular communications between malignant T cells expressing macrophage migration inhibitory factor and macrophages and B cells expressing CD74.ABSTRACTCutaneous T-cell lymphoma (CTCL) is a rare cancer of skin-homing T cells. A subgroup of patients develops large cell transformation with rapid progression to an aggressive lymphoma. Here, we investigated the transformed CTCL (tCTCL) tumor ecosystem using integrative multiomics spanning whole-exome sequencing (WES), single-cell RNA sequencing, and immune profiling in a unique cohort of 56 patients. WES of 70 skin biopsies showed high tumor mutation burden, UV signatures that are prognostic for survival, exome-based driver events, and most recurrently mutated pathways in tCTCL. Single-cell profiling of 16 tCTCL skin biopsies identified a core oncogenic program with metabolic reprogramming toward oxidative phosphorylation (OXPHOS), cellular plasticity, upregulation of MYC and E2F activities, and downregulation of MHC I suggestive of immune escape. Pharmacologic perturbation using OXPHOS and MYC inhibitors demonstrated potent antitumor activities, whereas immune profiling provided in situ evidence of intercellular communications between malignant T cells expressing macrophage migration inhibitory factor and macrophages and B cells expressing CD74.Our study contributes a key resource to the community with the largest collection of tCTCL biopsies that are difficult to obtain. The multiomics data herein provide the first comprehensive compendium of genomic alterations in tCTCL and identify potential prognostic signatures and novel therapeutic targets for an incurable T-cell lymphoma. This article is highlighted in the In This Issue feature, p. 1171.SIGNIFICANCEOur study contributes a key resource to the community with the largest collection of tCTCL biopsies that are difficult to obtain. The multiomics data herein provide the first comprehensive compendium of genomic alterations in tCTCL and identify potential prognostic signatures and novel therapeutic targets for an incurable T-cell lymphoma. This article is highlighted in the In This Issue feature, p. 1171. Cutaneous T-cell lymphoma (CTCL) is a rare cancer of skin-homing T cells. A subgroup of patients develops large cell transformation with rapid progression to an aggressive lymphoma. Here, we investigated the transformed CTCL (tCTCL) tumor ecosystem using integrative multiomics spanning whole-exome sequencing (WES), single-cell RNA sequencing, and immune profiling in a unique cohort of 56 patients. WES of 70 skin biopsies showed high tumor mutation burden, UV signatures that are prognostic for survival, exome-based driver events, and most recurrently mutated pathways in tCTCL. Single-cell profiling of 16 tCTCL skin biopsies identified a core oncogenic program with metabolic reprogramming toward oxidative phosphorylation (OXPHOS), cellular plasticity, upregulation of MYC and E2F activities, and downregulation of MHC I suggestive of immune escape. Pharmacologic perturbation using OXPHOS and MYC inhibitors demonstrated potent antitumor activities, whereas immune profiling provided in situ evidence of intercellular communications between malignant T cells expressing macrophage migration inhibitory factor and macrophages and B cells expressing CD74. Our study contributes a key resource to the community with the largest collection of tCTCL biopsies that are difficult to obtain. The multiomics data herein provide the first comprehensive compendium of genomic alterations in tCTCL and identify potential prognostic signatures and novel therapeutic targets for an incurable T-cell lymphoma. This article is highlighted in the In This Issue feature, p. 1171. Cutaneous T-cell lymphoma is a rare cancer of skin-homing T-cells. A subgroup of patients develops large cell transformation with rapid progression to an aggressive lymphoma. Here, we investigated the transformed CTCL (tCTCL) tumor ecosystem using integrative multiomics spanning whole exome sequencing (WES), single-cell RNA-seq and immune profiling in a unique cohort of 56 patients. WES of 70 skin biopsies showed high tumor mutation burden, UV signatures that are prognostic for survival, exome-based driver events and most recurrently mutated pathways in tCTCL. Single-cell profiling of 16 tCTCL skin biopsies identified a core oncogenic program with metabolic reprogramming toward oxidative phosphorylation, cellular plasticity, upregulation of MYC and E2F activities and down-regulation of MHC-I suggestive of immune escape. Pharmacologic perturbation using OXPHOS and MYC inhibitors demonstrated potent anti-tumor activities, while immune profiling provided in situ evidence of intercellular communications between malignant T-cells expressing macrophage migration inhibitory factor and macrophages and B-cells expressing CD74. |
| Author | Zhang, Xiaohui Nguyen, Jonathan V. Harro, Carly M. Chang, Shiun Harkins, Andrea Berglund, Anders Tordesillas, Leticia Sayegh, Zena Yoder, Sean Rodriguez, Paulo C. Messina, Jane L. Tsai, Kenneth Y. Whiddon, Shannen Seminario-Vidal, Lucia Song, Xingzhi Zhao, Yun Zhang, Jianhua Mulé, James J. Segura, Carlos Moran Reed, Rhianna A. Conejo-Garcia, José R. Song, Xiaofei de Mingo Pulido, Alvaro Chen, Pei-Ling Futreal, Andrew P. Zhang, Chaomei Sokol, Lubomir |
| AuthorAffiliation | 3 Department of Cutaneous Oncology, H. Lee Moffitt Cancer Center and Research Institute, Tampa, Florida, USA 9 Department of Biopharma Services, Admera Health, Holmdel, NJ, USA 1 Department of Genomic Medicine, The UT MD Anderson Cancer Center, Houston, TX, USA 8 Tissue Core Facility, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL, USA 4 Department of Tumor Biology, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL, USA 11 Department of Biostatistics and Bioinformatics, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL, USA 2 Department of Immunology, H. Lee Moffitt Cancer Center and Research Institute, Tampa, Florida, USA 5 Department of Malignant Hematology, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL, USA 10 Department of Pathology, H. Lee Moffitt Cancer Center and Research Institute, Tampa, Florida, USA 6 Advanced Analytical and Digital Laboratory, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL, USA 7 Molecular Geno |
| AuthorAffiliation_xml | – name: 4 Department of Tumor Biology, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL, USA – name: 6 Advanced Analytical and Digital Laboratory, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL, USA – name: 8 Tissue Core Facility, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL, USA – name: 11 Department of Biostatistics and Bioinformatics, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL, USA – name: 3 Department of Cutaneous Oncology, H. Lee Moffitt Cancer Center and Research Institute, Tampa, Florida, USA – name: 5 Department of Malignant Hematology, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL, USA – name: 1 Department of Genomic Medicine, The UT MD Anderson Cancer Center, Houston, TX, USA – name: 10 Department of Pathology, H. Lee Moffitt Cancer Center and Research Institute, Tampa, Florida, USA – name: 2 Department of Immunology, H. Lee Moffitt Cancer Center and Research Institute, Tampa, Florida, USA – name: 7 Molecular Genomics Core Facility, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL, USA – name: 9 Department of Biopharma Services, Admera Health, Holmdel, NJ, USA |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 These authors jointly supervised this work. AUTHOR CONTRIBUTIONS Conceptualization: P.L.C., K.Y.T, J.J.M, X.S.; Methodologies: P.L.C., X.S., K.Y.T, J.Z., P.A.F., P.C.R., S.C.; Computational / Bioinformatics Analysis: X.S., PLC, X.S., J.Z., P.A.F.; Investigation: P.L.C., X.S., S.C., A.M.P., L.T., J.N., C.M.S., C.Z., S.Y., Z.S., Resources: P.L.C., K.Y.T., J.Z., P.A.F., J.J.M., P.C.R., L.S.V., L.S., R.A.R., A.F.H., S.W., J.L.J., Z.S., Y.Z.; Clinical data review: P.L.C., L.S.V.; Writing: P.L.C., X.S., S.C.; Writing – review: P.L.C., K.Y.T, P.A.F., A.B., J.R.C., C.H., L.S.V., J.L.M.; Visualization: X.S., P.L.C., K.Y.T., A. B.; Supervision: P.L.C., K.Y.T., J.Z.. Funding Acquisition: P.L.C., J.J.M. Review and approval of the final manuscript was provided by all authors. These authors contributed equally to this work, interchangeable |
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| Snippet | Cutaneous T-cell lymphoma (CTCL) is a rare cancer of skin-homing T cells. A subgroup of patients develops large cell transformation with rapid progression to... Cutaneous T-cell lymphoma is a rare cancer of skin-homing T-cells. A subgroup of patients develops large cell transformation with rapid progression to an... |
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| SubjectTerms | Cell Transformation, Neoplastic Ecosystem Genomics Humans Lymphoma, T-Cell, Cutaneous - drug therapy Lymphoma, T-Cell, Cutaneous - genetics Skin Neoplasms - drug therapy Skin Neoplasms - genetics Skin Neoplasms - metabolism |
| Title | Genomic and Single-Cell Landscape Reveals Novel Drivers and Therapeutic Vulnerabilities of Transformed Cutaneous T-cell Lymphoma |
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