Characterization of the immunophenotypes and antigenomes of colorectal cancers reveals distinct tumor escape mechanisms and novel targets for immunotherapy
Background While large-scale cancer genomic projects are comprehensively characterizing the mutational spectrum of various cancers, so far little attention has been devoted to either define the antigenicity of these mutations or to characterize the immune responses they elicit. Here we present a str...
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| Vydané v: | Genome Biology Ročník 16; číslo 1; s. 64 |
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| Hlavní autori: | , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | English |
| Vydavateľské údaje: |
London
BioMed Central
31.03.2015
Springer Nature B.V |
| Predmet: | |
| ISSN: | 1465-6906, 1474-7596, 1474-760X, 1465-6906, 1474-760X, 1465-6914 |
| On-line prístup: | Získať plný text |
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| Abstract | Background
While large-scale cancer genomic projects are comprehensively characterizing the mutational spectrum of various cancers, so far little attention has been devoted to either define the antigenicity of these mutations or to characterize the immune responses they elicit. Here we present a strategy to characterize the immunophenotypes and the antigen-ome of human colorectal cancer.
Results
We apply our strategy to a large colorectal cancer cohort (n = 598) and show that subpopulations of tumor-infiltrating lymphocytes are associated with distinct molecular phenotypes. The characterization of the antigenome shows that a large number of cancer-germline antigens are expressed in all patients. In contrast, neo-antigens are rarely shared between patients, indicating that cancer vaccination requires individualized strategy. Analysis of the genetic basis of the tumors reveals distinct tumor escape mechanisms for the patient subgroups. Hypermutated tumors are depleted of immunosuppressive cells and show upregulation of immunoinhibitory molecules. Non-hypermutated tumors are enriched with immunosuppressive cells, and the expression of immunoinhibitors and MHC molecules is downregulated. Reconstruction of the interaction network of tumor-infiltrating lymphocytes and immunomodulatory molecules followed by a validation with 11 independent cohorts (n = 1,945) identifies BCMA as a novel druggable target. Finally, linear regression modeling identifies major determinants of tumor immunogenicity, which include well-characterized modulators as well as a novel candidate, CCR8, which is then tested in an orthologous immunodeficient mouse model.
Conclusions
The immunophenotypes of the tumors and the cancer antigenome remain widely unexplored, and our findings represent a step toward the development of personalized cancer immunotherapies. |
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| AbstractList | Background While large-scale cancer genomic projects are comprehensively characterizing the mutational spectrum of various cancers, so far little attention has been devoted to either define the antigenicity of these mutations or to characterize the immune responses they elicit. Here we present a strategy to characterize the immunophenotypes and the antigen-ome of human colorectal cancer. Results We apply our strategy to a large colorectal cancer cohort (n = 598) and show that subpopulations of tumor-infiltrating lymphocytes are associated with distinct molecular phenotypes. The characterization of the antigenome shows that a large number of cancer-germline antigens are expressed in all patients. In contrast, neo-antigens are rarely shared between patients, indicating that cancer vaccination requires individualized strategy. Analysis of the genetic basis of the tumors reveals distinct tumor escape mechanisms for the patient subgroups. Hypermutated tumors are depleted of immunosuppressive cells and show upregulation of immunoinhibitory molecules. Non-hypermutated tumors are enriched with immunosuppressive cells, and the expression of immunoinhibitors and MHC molecules is downregulated. Reconstruction of the interaction network of tumor-infiltrating lymphocytes and immunomodulatory molecules followed by a validation with 11 independent cohorts (n = 1,945) identifies BCMA as a novel druggable target. Finally, linear regression modeling identifies major determinants of tumor immunogenicity, which include well-characterized modulators as well as a novel candidate, CCR8, which is then tested in an orthologous immunodeficient mouse model. Conclusions The immunophenotypes of the tumors and the cancer antigenome remain widely unexplored, and our findings represent a step toward the development of personalized cancer immunotherapies. While large-scale cancer genomic projects are comprehensively characterizing the mutational spectrum of various cancers, so far little attention has been devoted to either define the antigenicity of these mutations or to characterize the immune responses they elicit. Here we present a strategy to characterize the immunophenotypes and the antigen-ome of human colorectal cancer.BACKGROUNDWhile large-scale cancer genomic projects are comprehensively characterizing the mutational spectrum of various cancers, so far little attention has been devoted to either define the antigenicity of these mutations or to characterize the immune responses they elicit. Here we present a strategy to characterize the immunophenotypes and the antigen-ome of human colorectal cancer.We apply our strategy to a large colorectal cancer cohort (n = 598) and show that subpopulations of tumor-infiltrating lymphocytes are associated with distinct molecular phenotypes. The characterization of the antigenome shows that a large number of cancer-germline antigens are expressed in all patients. In contrast, neo-antigens are rarely shared between patients, indicating that cancer vaccination requires individualized strategy. Analysis of the genetic basis of the tumors reveals distinct tumor escape mechanisms for the patient subgroups. Hypermutated tumors are depleted of immunosuppressive cells and show upregulation of immunoinhibitory molecules. Non-hypermutated tumors are enriched with immunosuppressive cells, and the expression of immunoinhibitors and MHC molecules is downregulated. Reconstruction of the interaction network of tumor-infiltrating lymphocytes and immunomodulatory molecules followed by a validation with 11 independent cohorts (n = 1,945) identifies BCMA as a novel druggable target. Finally, linear regression modeling identifies major determinants of tumor immunogenicity, which include well-characterized modulators as well as a novel candidate, CCR8, which is then tested in an orthologous immunodeficient mouse model.RESULTSWe apply our strategy to a large colorectal cancer cohort (n = 598) and show that subpopulations of tumor-infiltrating lymphocytes are associated with distinct molecular phenotypes. The characterization of the antigenome shows that a large number of cancer-germline antigens are expressed in all patients. In contrast, neo-antigens are rarely shared between patients, indicating that cancer vaccination requires individualized strategy. Analysis of the genetic basis of the tumors reveals distinct tumor escape mechanisms for the patient subgroups. Hypermutated tumors are depleted of immunosuppressive cells and show upregulation of immunoinhibitory molecules. Non-hypermutated tumors are enriched with immunosuppressive cells, and the expression of immunoinhibitors and MHC molecules is downregulated. Reconstruction of the interaction network of tumor-infiltrating lymphocytes and immunomodulatory molecules followed by a validation with 11 independent cohorts (n = 1,945) identifies BCMA as a novel druggable target. Finally, linear regression modeling identifies major determinants of tumor immunogenicity, which include well-characterized modulators as well as a novel candidate, CCR8, which is then tested in an orthologous immunodeficient mouse model.The immunophenotypes of the tumors and the cancer antigenome remain widely unexplored, and our findings represent a step toward the development of personalized cancer immunotherapies.CONCLUSIONSThe immunophenotypes of the tumors and the cancer antigenome remain widely unexplored, and our findings represent a step toward the development of personalized cancer immunotherapies. While large-scale cancer genomic projects are comprehensively characterizing the mutational spectrum of various cancers, so far little attention has been devoted to either define the antigenicity of these mutations or to characterize the immune responses they elicit. Here we present a strategy to characterize the immunophenotypes and the antigen-ome of human colorectal cancer. We apply our strategy to a large colorectal cancer cohort (n = 598) and show that subpopulations of tumor-infiltrating lymphocytes are associated with distinct molecular phenotypes. The characterization of the antigenome shows that a large number of cancer-germline antigens are expressed in all patients. In contrast, neo-antigens are rarely shared between patients, indicating that cancer vaccination requires individualized strategy. Analysis of the genetic basis of the tumors reveals distinct tumor escape mechanisms for the patient subgroups. Hypermutated tumors are depleted of immunosuppressive cells and show upregulation of immunoinhibitory molecules. Non-hypermutated tumors are enriched with immunosuppressive cells, and the expression of immunoinhibitors and MHC molecules is downregulated. Reconstruction of the interaction network of tumor-infiltrating lymphocytes and immunomodulatory molecules followed by a validation with 11 independent cohorts (n = 1,945) identifies BCMA as a novel druggable target. Finally, linear regression modeling identifies major determinants of tumor immunogenicity, which include well-characterized modulators as well as a novel candidate, CCR8, which is then tested in an orthologous immunodeficient mouse model. The immunophenotypes of the tumors and the cancer antigenome remain widely unexplored, and our findings represent a step toward the development of personalized cancer immunotherapies. Background While large-scale cancer genomic projects are comprehensively characterizing the mutational spectrum of various cancers, so far little attention has been devoted to either define the antigenicity of these mutations or to characterize the immune responses they elicit. Here we present a strategy to characterize the immunophenotypes and the antigen-ome of human colorectal cancer. Results We apply our strategy to a large colorectal cancer cohort (n = 598) and show that subpopulations of tumor-infiltrating lymphocytes are associated with distinct molecular phenotypes. The characterization of the antigenome shows that a large number of cancer-germline antigens are expressed in all patients. In contrast, neo-antigens are rarely shared between patients, indicating that cancer vaccination requires individualized strategy. Analysis of the genetic basis of the tumors reveals distinct tumor escape mechanisms for the patient subgroups. Hypermutated tumors are depleted of immunosuppressive cells and show upregulation of immunoinhibitory molecules. Non-hypermutated tumors are enriched with immunosuppressive cells, and the expression of immunoinhibitors and MHC molecules is downregulated. Reconstruction of the interaction network of tumor-infiltrating lymphocytes and immunomodulatory molecules followed by a validation with 11 independent cohorts (n = 1,945) identifies BCMA as a novel druggable target. Finally, linear regression modeling identifies major determinants of tumor immunogenicity, which include well-characterized modulators as well as a novel candidate, CCR8, which is then tested in an orthologous immunodeficient mouse model. Conclusions The immunophenotypes of the tumors and the cancer antigenome remain widely unexplored, and our findings represent a step toward the development of personalized cancer immunotherapies. |
| ArticleNumber | 64 |
| Author | Charoentong, Pornpimol Fischer, Maria L Hackl, Hubert Snajder, Rene Krogsdam, Anne M Angelova, Mihaela Bindea, Gabriela Waldner, Maximilian J Galon, Jerome Trajanoski, Zlatko Mlecnik, Bernhard |
| Author_xml | – sequence: 1 givenname: Mihaela surname: Angelova fullname: Angelova, Mihaela organization: Biocenter, Division of Bioinformatics, Medical University of Innsbruck – sequence: 2 givenname: Pornpimol surname: Charoentong fullname: Charoentong, Pornpimol organization: Biocenter, Division of Bioinformatics, Medical University of Innsbruck – sequence: 3 givenname: Hubert surname: Hackl fullname: Hackl, Hubert organization: Biocenter, Division of Bioinformatics, Medical University of Innsbruck – sequence: 4 givenname: Maria L surname: Fischer fullname: Fischer, Maria L organization: Biocenter, Division of Bioinformatics, Medical University of Innsbruck – sequence: 5 givenname: Rene surname: Snajder fullname: Snajder, Rene organization: Biocenter, Division of Bioinformatics, Medical University of Innsbruck – sequence: 6 givenname: Anne M surname: Krogsdam fullname: Krogsdam, Anne M organization: Biocenter, Division of Bioinformatics, Medical University of Innsbruck – sequence: 7 givenname: Maximilian J surname: Waldner fullname: Waldner, Maximilian J organization: Department of Medicine 1, University of Erlangen-Nuremberg – sequence: 8 givenname: Gabriela surname: Bindea fullname: Bindea, Gabriela organization: INSERM U872, Integrative Cancer Immunology Laboratory, Cordeliers Research Centre, Université Pierre et Marie Curie Paris 6 – sequence: 9 givenname: Bernhard surname: Mlecnik fullname: Mlecnik, Bernhard organization: INSERM U872, Integrative Cancer Immunology Laboratory, Cordeliers Research Centre, Université Pierre et Marie Curie Paris 6 – sequence: 10 givenname: Jerome surname: Galon fullname: Galon, Jerome organization: INSERM U872, Integrative Cancer Immunology Laboratory, Cordeliers Research Centre, Université Pierre et Marie Curie Paris 6 – sequence: 11 givenname: Zlatko surname: Trajanoski fullname: Trajanoski, Zlatko email: zlatko.trajanoski@i-med.ac.at organization: Biocenter, Division of Bioinformatics, Medical University of Innsbruck |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25853550$$D View this record in MEDLINE/PubMed https://hal.sorbonne-universite.fr/hal-01149718$$DView record in HAL |
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While large-scale cancer genomic projects are comprehensively characterizing the mutational spectrum of various cancers, so far little attention has... While large-scale cancer genomic projects are comprehensively characterizing the mutational spectrum of various cancers, so far little attention has been... Background While large-scale cancer genomic projects are comprehensively characterizing the mutational spectrum of various cancers, so far little attention has... BACKGROUND: While large-scale cancer genomic projects are comprehensively characterizing the mutational spectrum of various cancers, so far little attention... Background: While large-scale cancer genomic projects are comprehensively characterizing the mutational spectrum of various cancers, so far little attention... |
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| SubjectTerms | Animal Genetics and Genomics Animals Antigenicity Antigens Antigens, Neoplasm - genetics Antigens, Neoplasm - immunology Bioinformatics Biomedical and Life Sciences Cancer immunotherapy Cancer Vaccines - immunology Cancer Vaccines - therapeutic use CCR8 protein Colorectal cancer Colorectal carcinoma colorectal neoplasms Colorectal Neoplasms - genetics Colorectal Neoplasms - immunology Colorectal Neoplasms - pathology Colorectal Neoplasms - therapy Evolutionary Biology Gene expression Genetic analysis genome Genomes Genomics Genotype & phenotype Human Genetics Human health and pathology Humans Immune response Immunodeficiency Immunogenicity Immunomodulation Immunophenotyping immunosuppression Immunotherapy Life Sciences Lymphocytes Lymphocytes, Tumor-Infiltrating - immunology Major histocompatibility complex Medical prognosis Mice Microbial Genetics and Genomics Patients Peptides Phenotypes Plant Genetics and Genomics regression analysis Studies T cell receptors Tumor Escape - genetics Tumor Escape - immunology Tumor-infiltrating lymphocytes Tumors Vaccination Vaccines |
| Title | Characterization of the immunophenotypes and antigenomes of colorectal cancers reveals distinct tumor escape mechanisms and novel targets for immunotherapy |
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