High-dimensional cytometric analysis of colorectal cancer reveals novel mediators of antitumour immunity

ObjectiveA comprehensive understanding of anticancer immune responses is paramount for the optimal application and development of cancer immunotherapies. We unravelled local and systemic immune profiles in patients with colorectal cancer (CRC) by high-dimensional analysis to provide an unbiased char...

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Published in:	Gut Vol. 69; no. 4; pp. 691 - 703
Main Authors:	de Vries, Natasja L, van Unen, Vincent, Ijsselsteijn, Marieke E, Abdelaal, Tamim, van der Breggen, Ruud, Farina Sarasqueta, Arantza, Mahfouz, Ahmed, Peeters, Koen C M J, Höllt, Thomas, Lelieveldt, Boudewijn P F, Koning, Frits, de Miranda, Noel F C C
Format:	Journal Article
Language:	English
Published:	England BMJ Publishing Group Ltd and British Society of Gastroenterology 01.04.2020 BMJ Publishing Group LTD BMJ Publishing Group
Series:	Original research
Subjects:	Antibodies Antigens, CD - metabolism Cancer Cancer immunotherapy Cancer therapies Case-Control Studies CD103 antigen CD38 antigen CD56 antigen CD69 antigen CD7 antigen CD8 Antigens - metabolism Cells Clustering Colon Colonic Neoplasms - immunology Colonic Neoplasms - metabolism Colonic Neoplasms - pathology Colorectal cancer Colorectal carcinoma Cytotoxicity Flow Cytometry Genomics GI cancer Histocompatibility antigen HLA Humans immune landscape Immunity Immunofluorescence Immunogenicity Immunoglobulins Immunotherapy innate lymphoid cells Integrin alpha Chains - metabolism Lymph nodes Lymphatic system Lymphocyte Count Lymphocytes Lymphocytes T Lymphocytes, Tumor-Infiltrating mass cytometry Medical research Metastases Mismatch repair Mucosa Mutation Patients PD-1 protein Peripheral blood Phenotypes Principal components analysis Ribonucleic acid RNA single-cell immunophenotyping tissue-resident memory T cells Transcription Tumors Netherlands immune landscape colorectal cancer single-cell immunophenotyping innate lymphoid cells mass cytometry tissue-resident memory T cells
ISSN:	0017-5749, 1468-3288, 1468-3288
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Abstract	ObjectiveA comprehensive understanding of anticancer immune responses is paramount for the optimal application and development of cancer immunotherapies. We unravelled local and systemic immune profiles in patients with colorectal cancer (CRC) by high-dimensional analysis to provide an unbiased characterisation of the immune contexture of CRC.DesignThirty-six immune cell markers were simultaneously assessed at the single-cell level by mass cytometry in 35 CRC tissues, 26 tumour-associated lymph nodes, 17 colorectal healthy mucosa and 19 peripheral blood samples from 31 patients with CRC. Additionally, functional, transcriptional and spatial analyses of tumour-infiltrating lymphocytes were performed by flow cytometry, single-cell RNA-sequencing and multispectral immunofluorescence.ResultsWe discovered that a previously unappreciated innate lymphocyte population (Lin–CD7+CD127–CD56+CD45RO+) was enriched in CRC tissues and displayed cytotoxic activity. This subset demonstrated a tissue-resident (CD103+CD69+) phenotype and was most abundant in immunogenic mismatch repair (MMR)-deficient CRCs. Their presence in tumours was correlated with the infiltration of tumour-resident cytotoxic, helper and γδ T cells with highly similar activated (HLA-DR+CD38+PD-1+) phenotypes. Remarkably, activated γδ T cells were almost exclusively found in MMR-deficient cancers. Non-activated counterparts of tumour-resident cytotoxic and γδ T cells were present in CRC and healthy mucosa tissues, but not in lymph nodes, with the exception of tumour-positive lymph nodes.ConclusionThis work provides a blueprint for the understanding of the heterogeneous and intricate immune landscape of CRC, including the identification of previously unappreciated immune cell subsets. The concomitant presence of tumour-resident innate and adaptive immune cell populations suggests a multitargeted exploitation of their antitumour properties in a therapeutic setting.
AbstractList	ObjectiveA comprehensive understanding of anticancer immune responses is paramount for the optimal application and development of cancer immunotherapies. We unravelled local and systemic immune profiles in patients with colorectal cancer (CRC) by high-dimensional analysis to provide an unbiased characterisation of the immune contexture of CRC.DesignThirty-six immune cell markers were simultaneously assessed at the single-cell level by mass cytometry in 35 CRC tissues, 26 tumour-associated lymph nodes, 17 colorectal healthy mucosa and 19 peripheral blood samples from 31 patients with CRC. Additionally, functional, transcriptional and spatial analyses of tumour-infiltrating lymphocytes were performed by flow cytometry, single-cell RNA-sequencing and multispectral immunofluorescence.ResultsWe discovered that a previously unappreciated innate lymphocyte population (Lin–CD7+CD127–CD56+CD45RO+) was enriched in CRC tissues and displayed cytotoxic activity. This subset demonstrated a tissue-resident (CD103+CD69+) phenotype and was most abundant in immunogenic mismatch repair (MMR)-deficient CRCs. Their presence in tumours was correlated with the infiltration of tumour-resident cytotoxic, helper and γδ T cells with highly similar activated (HLA-DR+CD38+PD-1+) phenotypes. Remarkably, activated γδ T cells were almost exclusively found in MMR-deficient cancers. Non-activated counterparts of tumour-resident cytotoxic and γδ T cells were present in CRC and healthy mucosa tissues, but not in lymph nodes, with the exception of tumour-positive lymph nodes.ConclusionThis work provides a blueprint for the understanding of the heterogeneous and intricate immune landscape of CRC, including the identification of previously unappreciated immune cell subsets. The concomitant presence of tumour-resident innate and adaptive immune cell populations suggests a multitargeted exploitation of their antitumour properties in a therapeutic setting. A comprehensive understanding of anticancer immune responses is paramount for the optimal application and development of cancer immunotherapies. We unravelled local and systemic immune profiles in patients with colorectal cancer (CRC) by high-dimensional analysis to provide an unbiased characterisation of the immune contexture of CRC.OBJECTIVEA comprehensive understanding of anticancer immune responses is paramount for the optimal application and development of cancer immunotherapies. We unravelled local and systemic immune profiles in patients with colorectal cancer (CRC) by high-dimensional analysis to provide an unbiased characterisation of the immune contexture of CRC.Thirty-six immune cell markers were simultaneously assessed at the single-cell level by mass cytometry in 35 CRC tissues, 26 tumour-associated lymph nodes, 17 colorectal healthy mucosa and 19 peripheral blood samples from 31 patients with CRC. Additionally, functional, transcriptional and spatial analyses of tumour-infiltrating lymphocytes were performed by flow cytometry, single-cell RNA-sequencing and multispectral immunofluorescence.DESIGNThirty-six immune cell markers were simultaneously assessed at the single-cell level by mass cytometry in 35 CRC tissues, 26 tumour-associated lymph nodes, 17 colorectal healthy mucosa and 19 peripheral blood samples from 31 patients with CRC. Additionally, functional, transcriptional and spatial analyses of tumour-infiltrating lymphocytes were performed by flow cytometry, single-cell RNA-sequencing and multispectral immunofluorescence.We discovered that a previously unappreciated innate lymphocyte population (Lin-CD7+CD127-CD56+CD45RO+) was enriched in CRC tissues and displayed cytotoxic activity. This subset demonstrated a tissue-resident (CD103+CD69+) phenotype and was most abundant in immunogenic mismatch repair (MMR)-deficient CRCs. Their presence in tumours was correlated with the infiltration of tumour-resident cytotoxic, helper and γδ T cells with highly similar activated (HLA-DR+CD38+PD-1+) phenotypes. Remarkably, activated γδ T cells were almost exclusively found in MMR-deficient cancers. Non-activated counterparts of tumour-resident cytotoxic and γδ T cells were present in CRC and healthy mucosa tissues, but not in lymph nodes, with the exception of tumour-positive lymph nodes.RESULTSWe discovered that a previously unappreciated innate lymphocyte population (Lin-CD7+CD127-CD56+CD45RO+) was enriched in CRC tissues and displayed cytotoxic activity. This subset demonstrated a tissue-resident (CD103+CD69+) phenotype and was most abundant in immunogenic mismatch repair (MMR)-deficient CRCs. Their presence in tumours was correlated with the infiltration of tumour-resident cytotoxic, helper and γδ T cells with highly similar activated (HLA-DR+CD38+PD-1+) phenotypes. Remarkably, activated γδ T cells were almost exclusively found in MMR-deficient cancers. Non-activated counterparts of tumour-resident cytotoxic and γδ T cells were present in CRC and healthy mucosa tissues, but not in lymph nodes, with the exception of tumour-positive lymph nodes.This work provides a blueprint for the understanding of the heterogeneous and intricate immune landscape of CRC, including the identification of previously unappreciated immune cell subsets. The concomitant presence of tumour-resident innate and adaptive immune cell populations suggests a multitargeted exploitation of their antitumour properties in a therapeutic setting.CONCLUSIONThis work provides a blueprint for the understanding of the heterogeneous and intricate immune landscape of CRC, including the identification of previously unappreciated immune cell subsets. The concomitant presence of tumour-resident innate and adaptive immune cell populations suggests a multitargeted exploitation of their antitumour properties in a therapeutic setting. A comprehensive understanding of anticancer immune responses is paramount for the optimal application and development of cancer immunotherapies. We unravelled local and systemic immune profiles in patients with colorectal cancer (CRC) by high-dimensional analysis to provide an unbiased characterisation of the immune contexture of CRC. Thirty-six immune cell markers were simultaneously assessed at the single-cell level by mass cytometry in 35 CRC tissues, 26 tumour-associated lymph nodes, 17 colorectal healthy mucosa and 19 peripheral blood samples from 31 patients with CRC. Additionally, functional, transcriptional and spatial analyses of tumour-infiltrating lymphocytes were performed by flow cytometry, single-cell RNA-sequencing and multispectral immunofluorescence. We discovered that a previously unappreciated innate lymphocyte population (Lin CD7 CD127 CD56 CD45RO ) was enriched in CRC tissues and displayed cytotoxic activity. This subset demonstrated a tissue-resident (CD103 CD69 ) phenotype and was most abundant in immunogenic mismatch repair (MMR)-deficient CRCs. Their presence in tumours was correlated with the infiltration of tumour-resident cytotoxic, helper and γδ T cells with highly similar activated (HLA-DR CD38 PD-1 ) phenotypes. Remarkably, activated γδ T cells were almost exclusively found in MMR-deficient cancers. Non-activated counterparts of tumour-resident cytotoxic and γδ T cells were present in CRC and healthy mucosa tissues, but not in lymph nodes, with the exception of tumour-positive lymph nodes. This work provides a blueprint for the understanding of the heterogeneous and intricate immune landscape of CRC, including the identification of previously unappreciated immune cell subsets. The concomitant presence of tumour-resident innate and adaptive immune cell populations suggests a multitargeted exploitation of their antitumour properties in a therapeutic setting.
Author	Lelieveldt, Boudewijn P F Ijsselsteijn, Marieke E Peeters, Koen C M J Abdelaal, Tamim Höllt, Thomas van der Breggen, Ruud de Vries, Natasja L Farina Sarasqueta, Arantza Mahfouz, Ahmed van Unen, Vincent Koning, Frits de Miranda, Noel F C C
AuthorAffiliation	2 TECObiosciences GmbH , Landshut , Germany 1 Immunohematology and Blood Transfusion , Leiden University Medical Center , Leiden , Netherlands 7 Computer Graphics and Visualization , Delft University of Technology , Delft , The Netherlands 3 Pathology , Leiden University Medical Center , Leiden , The Netherlands 6 Surgery , Leiden University Medical Center , Leiden , The Netherlands 4 Pattern Recognition and Bioinformatics , Delft University of Technology , Delft , The Netherlands 5 Leiden Computational Biology Center , Leiden University Medical Center , Leiden , The Netherlands 8 LKEB Radiology , Leiden University Medical Center , Leiden , The Netherlands
AuthorAffiliation_xml	– name: 8 LKEB Radiology , Leiden University Medical Center , Leiden , The Netherlands – name: 4 Pattern Recognition and Bioinformatics , Delft University of Technology , Delft , The Netherlands – name: 1 Immunohematology and Blood Transfusion , Leiden University Medical Center , Leiden , Netherlands – name: 7 Computer Graphics and Visualization , Delft University of Technology , Delft , The Netherlands – name: 2 TECObiosciences GmbH , Landshut , Germany – name: 3 Pathology , Leiden University Medical Center , Leiden , The Netherlands – name: 5 Leiden Computational Biology Center , Leiden University Medical Center , Leiden , The Netherlands – name: 6 Surgery , Leiden University Medical Center , Leiden , The Netherlands
Author_xml	– sequence: 1 givenname: Natasja L orcidid: 0000-0003-4966-7036 surname: de Vries fullname: de Vries, Natasja L organization: TECObiosciences GmbH, Landshut, Germany – sequence: 2 givenname: Vincent surname: van Unen fullname: van Unen, Vincent organization: Immunohematology and Blood Transfusion, Leiden University Medical Center, Leiden, Netherlands – sequence: 3 givenname: Marieke E surname: Ijsselsteijn fullname: Ijsselsteijn, Marieke E organization: Pathology, Leiden University Medical Center, Leiden, The Netherlands – sequence: 4 givenname: Tamim surname: Abdelaal fullname: Abdelaal, Tamim organization: Leiden Computational Biology Center, Leiden University Medical Center, Leiden, The Netherlands – sequence: 5 givenname: Ruud surname: van der Breggen fullname: van der Breggen, Ruud organization: Pathology, Leiden University Medical Center, Leiden, The Netherlands – sequence: 6 givenname: Arantza surname: Farina Sarasqueta fullname: Farina Sarasqueta, Arantza organization: Pathology, Leiden University Medical Center, Leiden, The Netherlands – sequence: 7 givenname: Ahmed surname: Mahfouz fullname: Mahfouz, Ahmed organization: Leiden Computational Biology Center, Leiden University Medical Center, Leiden, The Netherlands – sequence: 8 givenname: Koen C M J surname: Peeters fullname: Peeters, Koen C M J organization: Surgery, Leiden University Medical Center, Leiden, The Netherlands – sequence: 9 givenname: Thomas surname: Höllt fullname: Höllt, Thomas organization: Computer Graphics and Visualization, Delft University of Technology, Delft, The Netherlands – sequence: 10 givenname: Boudewijn P F surname: Lelieveldt fullname: Lelieveldt, Boudewijn P F organization: LKEB Radiology, Leiden University Medical Center, Leiden, The Netherlands – sequence: 11 givenname: Frits surname: Koning fullname: Koning, Frits organization: Immunohematology and Blood Transfusion, Leiden University Medical Center, Leiden, Netherlands – sequence: 12 givenname: Noel F C C surname: de Miranda fullname: de Miranda, Noel F C C organization: Pathology, Leiden University Medical Center, Leiden, The Netherlands
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/31270164$$D View this record in MEDLINE/PubMed
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Keywords	immune landscape colorectal cancer single-cell immunophenotyping innate lymphoid cells mass cytometry tissue-resident memory T cells
Language	English
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16 Le, Durham, Smith 2017; 357 2024111023102747000_69.4.691.43 2024111023102747000_69.4.691.44 2024111023102747000_69.4.691.41 2024111023102747000_69.4.691.42 Middha (2024111023102747000_69.4.691.56) 2019; 3 2024111023102747000_69.4.691.49 2024111023102747000_69.4.691.47 2024111023102747000_69.4.691.48 2024111023102747000_69.4.691.45 2024111023102747000_69.4.691.46 2024111023102747000_69.4.691.10 2024111023102747000_69.4.691.54 2024111023102747000_69.4.691.11 2024111023102747000_69.4.691.55 2024111023102747000_69.4.691.52 2024111023102747000_69.4.691.53 2024111023102747000_69.4.691.50 2024111023102747000_69.4.691.51 2024111023102747000_69.4.691.18 Dierssen (2024111023102747000_69.4.691.40) 2007; 7 2024111023102747000_69.4.691.19 2024111023102747000_69.4.691.16 2024111023102747000_69.4.691.17 2024111023102747000_69.4.691.14 2024111023102747000_69.4.691.15 2024111023102747000_69.4.691.13 2024111023102747000_69.4.691.21 2024111023102747000_69.4.691.22 2024111023102747000_69.4.691.20 Kotecha (2024111023102747000_69.4.691.12) 2010; Chapter 10 2024111023102747000_69.4.691.1 2024111023102747000_69.4.691.2 2024111023102747000_69.4.691.3 2024111023102747000_69.4.691.4 2024111023102747000_69.4.691.5 2024111023102747000_69.4.691.6 2024111023102747000_69.4.691.7 2024111023102747000_69.4.691.29 2024111023102747000_69.4.691.8 2024111023102747000_69.4.691.9 2024111023102747000_69.4.691.27 2024111023102747000_69.4.691.28 2024111023102747000_69.4.691.25 2024111023102747000_69.4.691.26 2024111023102747000_69.4.691.23 2024111023102747000_69.4.691.24 2024111023102747000_69.4.691.32 2024111023102747000_69.4.691.33 2024111023102747000_69.4.691.30 2024111023102747000_69.4.691.31 2024111023102747000_69.4.691.38 2024111023102747000_69.4.691.39 2024111023102747000_69.4.691.36 2024111023102747000_69.4.691.37 2024111023102747000_69.4.691.34 2024111023102747000_69.4.691.35 32139551 - Gut. 2020 Dec;69(12):2261-2263
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Snippet	ObjectiveA comprehensive understanding of anticancer immune responses is paramount for the optimal application and development of cancer immunotherapies. We... A comprehensive understanding of anticancer immune responses is paramount for the optimal application and development of cancer immunotherapies. We unravelled...
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SubjectTerms	Antibodies Antigens, CD - metabolism Cancer Cancer immunotherapy Cancer therapies Case-Control Studies CD103 antigen CD38 antigen CD56 antigen CD69 antigen CD7 antigen CD8 Antigens - metabolism Cells Clustering Colon Colonic Neoplasms - immunology Colonic Neoplasms - metabolism Colonic Neoplasms - pathology Colorectal cancer Colorectal carcinoma Cytotoxicity Flow Cytometry Genomics GI cancer Histocompatibility antigen HLA Humans immune landscape Immunity Immunofluorescence Immunogenicity Immunoglobulins Immunotherapy innate lymphoid cells Integrin alpha Chains - metabolism Lymph nodes Lymphatic system Lymphocyte Count Lymphocytes Lymphocytes T Lymphocytes, Tumor-Infiltrating mass cytometry Medical research Metastases Mismatch repair Mucosa Mutation Patients PD-1 protein Peripheral blood Phenotypes Principal components analysis Ribonucleic acid RNA single-cell immunophenotyping tissue-resident memory T cells Transcription Tumors
Title	High-dimensional cytometric analysis of colorectal cancer reveals novel mediators of antitumour immunity
URI	https://gut.bmj.com/content/early/2019/07/03/gutjnl-2019-318672.full https://gut.bmj.com/content/69/4/691.full https://www.ncbi.nlm.nih.gov/pubmed/31270164 https://www.proquest.com/docview/2372615901 https://www.proquest.com/docview/3176094286 https://www.proquest.com/docview/2252266669 https://pubmed.ncbi.nlm.nih.gov/PMC7063399
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