Oncogenic states dictate the prognostic and predictive connotations of intratumoral immune response

BackgroundAn immune active cancer phenotype typified by a T helper 1 (Th-1) immune response has been associated with increased responsiveness to immunotherapy and favorable prognosis in some but not all cancer types. The reason of this differential prognostic connotation remains unknown.MethodsTo ex...

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Published inJournal for immunotherapy of cancer Vol. 8; no. 1; p. e000617
Main Authors Roelands, Jessica, Hendrickx, Wouter, Zoppoli, Gabriele, Mall, Raghvendra, Saad, Mohamad, Halliwill, Kyle, Curigliano, Giuseppe, Rinchai, Darawan, Decock, Julie, Delogu, Lucia G, Turan, Tolga, Samayoa, Josue, Chouchane, Lotfi, Ballestrero, Alberto, Wang, Ena, Finetti, Pascal, Bertucci, Francois, Miller, Lance D, Galon, Jerome, Marincola, Francesco M, Kuppen, Peter J K, Ceccarelli, Michele, Bedognetti, Davide
Format Journal Article
LanguageEnglish
Published England BMJ Publishing Group LTD 01.04.2020
BMJ Publishing Group
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Abstract BackgroundAn immune active cancer phenotype typified by a T helper 1 (Th-1) immune response has been associated with increased responsiveness to immunotherapy and favorable prognosis in some but not all cancer types. The reason of this differential prognostic connotation remains unknown.MethodsTo explore the contextual prognostic value of cancer immune phenotypes, we applied a multimodal pan-cancer analysis among 31 different histologies (9282 patients), encompassing immune and oncogenic transcriptomic analysis, mutational and neoantigen load and copy number variations.ResultsWe demonstrated that the favorable prognostic connotation conferred by the presence of a Th-1 immune response was abolished in tumors displaying specific tumor-cell intrinsic attributes such as high transforming growth factor-beta (TGF-β) signaling and low proliferation capacity. This observation was independent of mutation rate. We validated this observation in the context of immune checkpoint inhibition. WNT-β catenin, barrier molecules, Notch, hedgehog, mismatch repair, telomerase activity and AMPK signaling were the pathways most coherently associated with an immune silent phenotype together with mutations of driver genes including IDH1/2, FOXA2, HDAC3, PSIP1, MAP3K1, KRAS, NRAS, EGFR, FGFR3, WNT5A and IRF7.ConclusionsThis is the first systematic study demonstrating that the prognostic and predictive role of a bona fide favorable intratumoral immune response is dependent on the disposition of specific oncogenic pathways. This information could be used to refine stratification algorithms and prioritize hierarchically relevant targets for combination therapies.
AbstractList BackgroundAn immune active cancer phenotype typified by a T helper 1 (Th-1) immune response has been associated with increased responsiveness to immunotherapy and favorable prognosis in some but not all cancer types. The reason of this differential prognostic connotation remains unknown.MethodsTo explore the contextual prognostic value of cancer immune phenotypes, we applied a multimodal pan-cancer analysis among 31 different histologies (9282 patients), encompassing immune and oncogenic transcriptomic analysis, mutational and neoantigen load and copy number variations.ResultsWe demonstrated that the favorable prognostic connotation conferred by the presence of a Th-1 immune response was abolished in tumors displaying specific tumor-cell intrinsic attributes such as high transforming growth factor-beta (TGF-β) signaling and low proliferation capacity. This observation was independent of mutation rate. We validated this observation in the context of immune checkpoint inhibition. WNT-β catenin, barrier molecules, Notch, hedgehog, mismatch repair, telomerase activity and AMPK signaling were the pathways most coherently associated with an immune silent phenotype together with mutations of driver genes including IDH1/2, FOXA2, HDAC3, PSIP1, MAP3K1, KRAS, NRAS, EGFR, FGFR3, WNT5A and IRF7.ConclusionsThis is the first systematic study demonstrating that the prognostic and predictive role of a bona fide favorable intratumoral immune response is dependent on the disposition of specific oncogenic pathways. This information could be used to refine stratification algorithms and prioritize hierarchically relevant targets for combination therapies.
Background An immune active cancer phenotype typified by a T helper 1 (Th-1) immune response has been associated with increased responsiveness to immunotherapy and favorable prognosis in some but not all cancer types. The reason of this differential prognostic connotation remains unknown.Methods To explore the contextual prognostic value of cancer immune phenotypes, we applied a multimodal pan-cancer analysis among 31 different histologies (9282 patients), encompassing immune and oncogenic transcriptomic analysis, mutational and neoantigen load and copy number variations.Results We demonstrated that the favorable prognostic connotation conferred by the presence of a Th-1 immune response was abolished in tumors displaying specific tumor-cell intrinsic attributes such as high transforming growth factor-beta (TGF-β) signaling and low proliferation capacity. This observation was independent of mutation rate. We validated this observation in the context of immune checkpoint inhibition. WNT-β catenin, barrier molecules, Notch, hedgehog, mismatch repair, telomerase activity and AMPK signaling were the pathways most coherently associated with an immune silent phenotype together with mutations of driver genes including IDH1/2, FOXA2, HDAC3, PSIP1, MAP3K1, KRAS, NRAS, EGFR, FGFR3, WNT5A and IRF7.Conclusions This is the first systematic study demonstrating that the prognostic and predictive role of a bona fide favorable intratumoral immune response is dependent on the disposition of specific oncogenic pathways. This information could be used to refine stratification algorithms and prioritize hierarchically relevant targets for combination therapies.
An immune active cancer phenotype typified by a T helper 1 (Th-1) immune response has been associated with increased responsiveness to immunotherapy and favorable prognosis in some but not all cancer types. The reason of this differential prognostic connotation remains unknown. To explore the contextual prognostic value of cancer immune phenotypes, we applied a multimodal pan-cancer analysis among 31 different histologies (9282 patients), encompassing immune and oncogenic transcriptomic analysis, mutational and neoantigen load and copy number variations. We demonstrated that the favorable prognostic connotation conferred by the presence of a Th-1 immune response was abolished in tumors displaying specific tumor-cell intrinsic attributes such as high transforming growth factor-beta (TGF-β) signaling and low proliferation capacity. This observation was independent of mutation rate. We validated this observation in the context of immune checkpoint inhibition. WNT- catenin, barrier molecules, Notch, hedgehog, mismatch repair, telomerase activity and AMPK signaling were the pathways most coherently associated with an immune silent phenotype together with mutations of driver genes including and . This is the first systematic study demonstrating that the prognostic and predictive role of a bona fide favorable intratumoral immune response is dependent on the disposition of specific oncogenic pathways. This information could be used to refine stratification algorithms and prioritize hierarchically relevant targets for combination therapies.
Author Samayoa, Josue
Mall, Raghvendra
Miller, Lance D
Chouchane, Lotfi
Ballestrero, Alberto
Curigliano, Giuseppe
Roelands, Jessica
Halliwill, Kyle
Delogu, Lucia G
Saad, Mohamad
Rinchai, Darawan
Decock, Julie
Turan, Tolga
Kuppen, Peter J K
Bertucci, Francois
Ceccarelli, Michele
Hendrickx, Wouter
Finetti, Pascal
Bedognetti, Davide
Zoppoli, Gabriele
Galon, Jerome
Wang, Ena
Marincola, Francesco M
AuthorAffiliation 4 IRCCS Ospedale Policlinico San Martino , Genova , Italy
6 Qatar Computing Research Institute (QCRI) , Hamad Bin Khalifa University (HBKU) , Doha , Qatar
21 Department of Electrical Engineering and Information Technology (DIETI) , University of Naples "Federico II" , Naples , Italy
15 Laboratoire d'Oncologie Prédictive , Centre de Recherche en Cancérologie de Marseille (CRCM), Institut Paoli-Calmettes, INSERM UMR1068, CNRS UMR725, Aix-Marseille Université , Marseille , France
19 Centre de Recherche des Cordeliers , Sorbonne Université, Sorbonne Paris Cité, Université de Paris , Paris , France
8 Department of Oncology and Hemato-Oncology , University of Milano , Milano , Italy
12 Istituto di Ricerca Pediatrica , Fondazione Città della Speranza , Padua , Italy
2 Department of Surgery , Leiden University Medical Center (LUMC) , Leiden , The Netherlands
10 Cancer Research Center , Qatar Biomedical Research Institute (QBRI), Hamad Bin Khalifa University (HBKU), Qatar Foundation (QF) , Doha , Qatar
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/32376723$$D View this record in MEDLINE/PubMed
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Issue 1
Keywords genome Instability
gene expression profiling
genetic markers
immunotherapy
cytotoxicity, immunologic
Language English
License This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited, appropriate credit is given, any changes made indicated, and the use is non-commercial. See http://creativecommons.org/licenses/by-nc/4.0/.
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PublicationTitle Journal for immunotherapy of cancer
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Snippet BackgroundAn immune active cancer phenotype typified by a T helper 1 (Th-1) immune response has been associated with increased responsiveness to immunotherapy...
An immune active cancer phenotype typified by a T helper 1 (Th-1) immune response has been associated with increased responsiveness to immunotherapy and...
BACKGROUNDAn immune active cancer phenotype typified by a T helper 1 (Th-1) immune response has been associated with increased responsiveness to immunotherapy...
Background An immune active cancer phenotype typified by a T helper 1 (Th-1) immune response has been associated with increased responsiveness to immunotherapy...
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StartPage e000617
SubjectTerms Breast cancer
Cancer
Classification
Clustering
Data analysis
Datasets
Female
Gene expression
Gene Expression Profiling - methods
Humans
Immunity - immunology
Immunology
Immunotherapy
Immunotherapy - methods
Immunotherapy Biomarkers
Life Sciences
Male
Melanoma
Metastasis
Mutation
Neoplasms - immunology
Neoplasms - mortality
Oncogenes - immunology
Prognosis
Survival Analysis
Tumors
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Title Oncogenic states dictate the prognostic and predictive connotations of intratumoral immune response
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