CD103 and CD39 coexpression identifies neoantigen-specific cytotoxic T cells in colorectal cancers with low mutation burden

BackgroundExpression of CD103 and CD39 has been found to pinpoint tumor-reactive CD8+ T cells in a variety of solid cancers. We aimed to investigate whether these markers specifically identify neoantigen-specific T cells in colorectal cancers (CRCs) with low mutation burden.Experimental designWhole-...

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Veröffentlicht in:	Journal for immunotherapy of cancer Jg. 11; H. 2; S. e005887
Hauptverfasser:	van den Bulk, Jitske, van der Ploeg, Manon, Ijsselsteijn, Marieke E, Ruano, Dina, van der Breggen, Ruud, Duhen, Rebekka, Peeters, Koen C M J, Fariña-Sarasqueta, Arantza, Verdegaal, Els M E, van der Burg, Sjoerd H, Duhen, Thomas, de Miranda, Noel F C C
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	England BMJ Publishing Group Ltd 01.02.2023 BMJ Publishing Group LTD BMJ Publishing Group
Schriftenreihe:	Original research
Schlagworte:	Antigens Basic Tumor Immunology Cancer CD8-Positive T-Lymphocytes Colorectal cancer Colorectal Neoplasms Cytotoxicity Gastrointestinal Neoplasms Humans Immunotherapy Lymphocytes Lymphocytes, Tumor-Infiltrating Mutation Patients Pharmacy Rectum T cell receptors T-Lymphocyte Subsets - pathology T-Lymphocytes, Cytotoxic Tumors Netherlands United Kingdom > UK United States > US Basel Switzerland Massachusetts England Switzerland CD8-Positive T-Lymphocytes Antigens Gastrointestinal Neoplasms Lymphocytes, Tumor-Infiltrating Immunotherapy
ISSN:	2051-1426, 2051-1426
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Abstract	BackgroundExpression of CD103 and CD39 has been found to pinpoint tumor-reactive CD8+ T cells in a variety of solid cancers. We aimed to investigate whether these markers specifically identify neoantigen-specific T cells in colorectal cancers (CRCs) with low mutation burden.Experimental designWhole-exome and RNA sequencing of 11 mismatch repair-proficient (MMR-proficient) CRCs and corresponding healthy tissues were performed to determine the presence of putative neoantigens. In parallel, tumor-infiltrating lymphocytes (TILs) were cultured from the tumor fragments and, in parallel, CD8+ T cells were flow-sorted from their respective tumor digests based on single or combined expression of CD103 and CD39. Each subset was expanded and subsequently interrogated for neoantigen-directed reactivity with synthetic peptides. Neoantigen-directed reactivity was determined by flow cytometric analyses of T cell activation markers and ELISA-based detection of IFN-γ and granzyme B release. Additionally, imaging mass cytometry was applied to investigate the localization of CD103+CD39+ cytotoxic T cells in tumors.ResultsNeoantigen-directed reactivity was only encountered in bulk TIL populations and CD103+CD39+ (double positive, DP) CD8+ T cell subsets but never in double-negative or single-positive subsets. Neoantigen-reactivity detected in bulk TIL but not in DP CD8+ T cells could be attributed to CD4+ T cells. CD8+ T cells that were located in direct contact with cancer cells in tumor tissues were enriched for CD103 and CD39 expression.ConclusionCoexpression of CD103 and CD39 is characteristic of neoantigen-specific CD8+ T cells in MMR-proficient CRCs with low mutation burden. The exploitation of these subsets in the context of adoptive T cell transfer or engineered T cell receptor therapies is a promising avenue to extend the benefits of immunotherapy to an increasing number of CRC patients.
AbstractList	Background Expression of CD103 and CD39 has been found to pinpoint tumor-reactive CD8+ T cells in a variety of solid cancers. We aimed to investigate whether these markers specifically identify neoantigen-specific T cells in colorectal cancers (CRCs) with low mutation burden.Experimental design Whole-exome and RNA sequencing of 11 mismatch repair-proficient (MMR-proficient) CRCs and corresponding healthy tissues were performed to determine the presence of putative neoantigens. In parallel, tumor-infiltrating lymphocytes (TILs) were cultured from the tumor fragments and, in parallel, CD8+ T cells were flow-sorted from their respective tumor digests based on single or combined expression of CD103 and CD39. Each subset was expanded and subsequently interrogated for neoantigen-directed reactivity with synthetic peptides. Neoantigen-directed reactivity was determined by flow cytometric analyses of T cell activation markers and ELISA-based detection of IFN-γ and granzyme B release. Additionally, imaging mass cytometry was applied to investigate the localization of CD103+CD39+ cytotoxic T cells in tumors.Results Neoantigen-directed reactivity was only encountered in bulk TIL populations and CD103+CD39+ (double positive, DP) CD8+ T cell subsets but never in double-negative or single-positive subsets. Neoantigen-reactivity detected in bulk TIL but not in DP CD8+ T cells could be attributed to CD4+ T cells. CD8+ T cells that were located in direct contact with cancer cells in tumor tissues were enriched for CD103 and CD39 expression.Conclusion Coexpression of CD103 and CD39 is characteristic of neoantigen-specific CD8+ T cells in MMR-proficient CRCs with low mutation burden. The exploitation of these subsets in the context of adoptive T cell transfer or engineered T cell receptor therapies is a promising avenue to extend the benefits of immunotherapy to an increasing number of CRC patients. Expression of CD103 and CD39 has been found to pinpoint tumor-reactive CD8+ T cells in a variety of solid cancers. We aimed to investigate whether these markers specifically identify neoantigen-specific T cells in colorectal cancers (CRCs) with low mutation burden.BACKGROUNDExpression of CD103 and CD39 has been found to pinpoint tumor-reactive CD8+ T cells in a variety of solid cancers. We aimed to investigate whether these markers specifically identify neoantigen-specific T cells in colorectal cancers (CRCs) with low mutation burden.Whole-exome and RNA sequencing of 11 mismatch repair-proficient (MMR-proficient) CRCs and corresponding healthy tissues were performed to determine the presence of putative neoantigens. In parallel, tumor-infiltrating lymphocytes (TILs) were cultured from the tumor fragments and, in parallel, CD8+ T cells were flow-sorted from their respective tumor digests based on single or combined expression of CD103 and CD39. Each subset was expanded and subsequently interrogated for neoantigen-directed reactivity with synthetic peptides. Neoantigen-directed reactivity was determined by flow cytometric analyses of T cell activation markers and ELISA-based detection of IFN-γ and granzyme B release. Additionally, imaging mass cytometry was applied to investigate the localization of CD103+CD39+ cytotoxic T cells in tumors.EXPERIMENTAL DESIGNWhole-exome and RNA sequencing of 11 mismatch repair-proficient (MMR-proficient) CRCs and corresponding healthy tissues were performed to determine the presence of putative neoantigens. In parallel, tumor-infiltrating lymphocytes (TILs) were cultured from the tumor fragments and, in parallel, CD8+ T cells were flow-sorted from their respective tumor digests based on single or combined expression of CD103 and CD39. Each subset was expanded and subsequently interrogated for neoantigen-directed reactivity with synthetic peptides. Neoantigen-directed reactivity was determined by flow cytometric analyses of T cell activation markers and ELISA-based detection of IFN-γ and granzyme B release. Additionally, imaging mass cytometry was applied to investigate the localization of CD103+CD39+ cytotoxic T cells in tumors.Neoantigen-directed reactivity was only encountered in bulk TIL populations and CD103+CD39+ (double positive, DP) CD8+ T cell subsets but never in double-negative or single-positive subsets. Neoantigen-reactivity detected in bulk TIL but not in DP CD8+ T cells could be attributed to CD4+ T cells. CD8+ T cells that were located in direct contact with cancer cells in tumor tissues were enriched for CD103 and CD39 expression.RESULTSNeoantigen-directed reactivity was only encountered in bulk TIL populations and CD103+CD39+ (double positive, DP) CD8+ T cell subsets but never in double-negative or single-positive subsets. Neoantigen-reactivity detected in bulk TIL but not in DP CD8+ T cells could be attributed to CD4+ T cells. CD8+ T cells that were located in direct contact with cancer cells in tumor tissues were enriched for CD103 and CD39 expression.Coexpression of CD103 and CD39 is characteristic of neoantigen-specific CD8+ T cells in MMR-proficient CRCs with low mutation burden. The exploitation of these subsets in the context of adoptive T cell transfer or engineered T cell receptor therapies is a promising avenue to extend the benefits of immunotherapy to an increasing number of CRC patients.CONCLUSIONCoexpression of CD103 and CD39 is characteristic of neoantigen-specific CD8+ T cells in MMR-proficient CRCs with low mutation burden. The exploitation of these subsets in the context of adoptive T cell transfer or engineered T cell receptor therapies is a promising avenue to extend the benefits of immunotherapy to an increasing number of CRC patients. BackgroundExpression of CD103 and CD39 has been found to pinpoint tumor-reactive CD8+ T cells in a variety of solid cancers. We aimed to investigate whether these markers specifically identify neoantigen-specific T cells in colorectal cancers (CRCs) with low mutation burden.Experimental designWhole-exome and RNA sequencing of 11 mismatch repair-proficient (MMR-proficient) CRCs and corresponding healthy tissues were performed to determine the presence of putative neoantigens. In parallel, tumor-infiltrating lymphocytes (TILs) were cultured from the tumor fragments and, in parallel, CD8+ T cells were flow-sorted from their respective tumor digests based on single or combined expression of CD103 and CD39. Each subset was expanded and subsequently interrogated for neoantigen-directed reactivity with synthetic peptides. Neoantigen-directed reactivity was determined by flow cytometric analyses of T cell activation markers and ELISA-based detection of IFN-γ and granzyme B release. Additionally, imaging mass cytometry was applied to investigate the localization of CD103+CD39+ cytotoxic T cells in tumors.ResultsNeoantigen-directed reactivity was only encountered in bulk TIL populations and CD103+CD39+ (double positive, DP) CD8+ T cell subsets but never in double-negative or single-positive subsets. Neoantigen-reactivity detected in bulk TIL but not in DP CD8+ T cells could be attributed to CD4+ T cells. CD8+ T cells that were located in direct contact with cancer cells in tumor tissues were enriched for CD103 and CD39 expression.ConclusionCoexpression of CD103 and CD39 is characteristic of neoantigen-specific CD8+ T cells in MMR-proficient CRCs with low mutation burden. The exploitation of these subsets in the context of adoptive T cell transfer or engineered T cell receptor therapies is a promising avenue to extend the benefits of immunotherapy to an increasing number of CRC patients. Expression of CD103 and CD39 has been found to pinpoint tumor-reactive CD8 T cells in a variety of solid cancers. We aimed to investigate whether these markers specifically identify neoantigen-specific T cells in colorectal cancers (CRCs) with low mutation burden. Whole-exome and RNA sequencing of 11 mismatch repair-proficient (MMR-proficient) CRCs and corresponding healthy tissues were performed to determine the presence of putative neoantigens. In parallel, tumor-infiltrating lymphocytes (TILs) were cultured from the tumor fragments and, in parallel, CD8 T cells were flow-sorted from their respective tumor digests based on single or combined expression of CD103 and CD39. Each subset was expanded and subsequently interrogated for neoantigen-directed reactivity with synthetic peptides. Neoantigen-directed reactivity was determined by flow cytometric analyses of T cell activation markers and ELISA-based detection of IFN-γ and granzyme B release. Additionally, imaging mass cytometry was applied to investigate the localization of CD103 CD39 cytotoxic T cells in tumors. Neoantigen-directed reactivity was only encountered in bulk TIL populations and CD103 CD39 (double positive, DP) CD8 T cell subsets but never in double-negative or single-positive subsets. Neoantigen-reactivity detected in bulk TIL but not in DP CD8 T cells could be attributed to CD4 T cells. CD8 T cells that were located in direct contact with cancer cells in tumor tissues were enriched for CD103 and CD39 expression. Coexpression of CD103 and CD39 is characteristic of neoantigen-specific CD8 T cells in MMR-proficient CRCs with low mutation burden. The exploitation of these subsets in the context of adoptive T cell transfer or engineered T cell receptor therapies is a promising avenue to extend the benefits of immunotherapy to an increasing number of CRC patients.
Author	Duhen, Thomas Duhen, Rebekka Verdegaal, Els M E Ijsselsteijn, Marieke E Fariña-Sarasqueta, Arantza Peeters, Koen C M J Ruano, Dina van der Ploeg, Manon van der Breggen, Ruud van den Bulk, Jitske van der Burg, Sjoerd H de Miranda, Noel F C C
AuthorAffiliation	1 Department of Pathology , Leiden University Medical Center , Leiden , The Netherlands 2 Basic Immunology Lab , Earle A Chiles Research Institute , Portland , Oregon , USA 3 Department of Surgery , Leiden University Medical Center , Leiden , The Netherlands 5 Anti-Cancer Immune Response Lab , Earle A Chiles Research Institute , Portland , Oregon , USA 4 Department of Medical Oncology, Oncode Institute , Leiden University Medical Center , Leiden , The Netherlands
AuthorAffiliation_xml	– name: 5 Anti-Cancer Immune Response Lab , Earle A Chiles Research Institute , Portland , Oregon , USA – name: 2 Basic Immunology Lab , Earle A Chiles Research Institute , Portland , Oregon , USA – name: 4 Department of Medical Oncology, Oncode Institute , Leiden University Medical Center , Leiden , The Netherlands – name: 3 Department of Surgery , Leiden University Medical Center , Leiden , The Netherlands – name: 1 Department of Pathology , Leiden University Medical Center , Leiden , The Netherlands
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Keywords	CD8-Positive T-Lymphocytes Antigens Gastrointestinal Neoplasms Lymphocytes, Tumor-Infiltrating Immunotherapy
Language	English
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PublicationDate	2023-02-01
PublicationDateYYYYMMDD	2023-02-01
PublicationDate_xml	– month: 02 year: 2023 text: 2023-02-01 day: 01
PublicationDecade	2020
PublicationPlace	England
PublicationPlace_xml	– name: England – name: London – name: BMA House, Tavistock Square, London, WC1H 9JR
PublicationSeriesTitle	Original research
PublicationTitle	Journal for immunotherapy of cancer
PublicationTitleAbbrev	J Immunother Cancer
PublicationTitleAlternate	J Immunother Cancer
PublicationYear	2023
Publisher	BMJ Publishing Group Ltd BMJ Publishing Group LTD BMJ Publishing Group
Publisher_xml	– name: BMJ Publishing Group Ltd – name: BMJ Publishing Group LTD – name: BMJ Publishing Group
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Snippet	BackgroundExpression of CD103 and CD39 has been found to pinpoint tumor-reactive CD8+ T cells in a variety of solid cancers. We aimed to investigate whether... Expression of CD103 and CD39 has been found to pinpoint tumor-reactive CD8 T cells in a variety of solid cancers. We aimed to investigate whether these markers... Expression of CD103 and CD39 has been found to pinpoint tumor-reactive CD8+ T cells in a variety of solid cancers. We aimed to investigate whether these... Background Expression of CD103 and CD39 has been found to pinpoint tumor-reactive CD8+ T cells in a variety of solid cancers. We aimed to investigate whether...
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SubjectTerms	Antigens Basic Tumor Immunology Cancer CD8-Positive T-Lymphocytes Colorectal cancer Colorectal Neoplasms Cytotoxicity Gastrointestinal Neoplasms Humans Immunotherapy Lymphocytes Lymphocytes, Tumor-Infiltrating Mutation Patients Pharmacy Rectum T cell receptors T-Lymphocyte Subsets - pathology T-Lymphocytes, Cytotoxic Tumors
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Title	CD103 and CD39 coexpression identifies neoantigen-specific cytotoxic T cells in colorectal cancers with low mutation burden
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