Tumor-specific T cells support chemokine-driven spatial organization of intratumoral immune microaggregates needed for long survival

BackgroundThe composition of the tumor immune microenvironment (TIME) associated with good prognosis generally also predicts the success of immunotherapy, and both entail the presence of pre-existing tumor-specific T cells. Here, the blueprint of the TIME associated with such an ongoing tumor-specif...

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Vydané v:Journal for immunotherapy of cancer Ročník 10; číslo 2; s. e004346
Hlavní autori: Abdulrahman, Ziena, Santegoets, Saskia J, Sturm, Gregor, Charoentong, Pornpimol, Ijsselsteijn, Marieke E, Somarakis, Antonios, Höllt, Thomas, Finotello, Francesca, Trajanoski, Zlatko, van Egmond, Sylvia L, Mustafa, Dana A M, Welters, Marij J P, de Miranda, Noel F C C, van der Burg, Sjoerd H
Médium: Journal Article
Jazyk:English
Vydavateľské údaje: England BMJ Publishing Group Ltd 01.02.2022
BMJ Publishing Group LTD
BMJ Publishing Group
Edícia:Original research
Predmet:
Antigens
Basic Tumor Immunology
Cancer
Cancer therapies
Chemokines - metabolism
Cytokines
Female
Gene expression
Head & neck cancer
Human papillomavirus
Humans
Immunotherapy
Lymphocytes
Male
Medical prognosis
Monitoring, Immunologic - methods
Patients
Quality control
Software
Squamous cell carcinoma
Surgery
T-Lymphocytes - metabolism
Throat cancer
tumor microenvironment
Tumor Microenvironment - immunology
Tumor necrosis factor-TNF
Tumors
United States > US
Netherlands
Germany
immunotherapy
tumor microenvironment
ISSN:2051-1426, 2051-1426
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Abstract BackgroundThe composition of the tumor immune microenvironment (TIME) associated with good prognosis generally also predicts the success of immunotherapy, and both entail the presence of pre-existing tumor-specific T cells. Here, the blueprint of the TIME associated with such an ongoing tumor-specific T-cell response was dissected in a unique prospective oropharyngeal squamous cell carcinoma (OPSCC) cohort, in which tumor-specific tumor-infiltrating T cells were detected (immune responsiveness (IR+)) or not (lack of immune responsiveness (IR−)).MethodsA comprehensive multimodal, high-dimensional strategy was applied to dissect the TIME of treatment-naive IR+ and IR− OPSCC tissue, including bulk RNA sequencing (NanoString), imaging mass cytometry (Hyperion) for phenotyping and spatial interaction analyses of immune cells, and combined single-cell gene expression profiling and T-cell receptor (TCR) sequencing (single-cell RNA sequencing (scRNAseq)) to characterize the transcriptional states of clonally expanded tumor-infiltrating T cells.ResultsIR+ patients had an excellent survival during >10 years follow-up. The tumors of IR+ patients expressed higher levels of genes strongly related to interferon gamma signaling, T-cell activation, TCR signaling, and mononuclear cell differentiation, as well as genes involved in several immune signaling pathways, than IR− patients. The top differently overexpressed genes included CXCL12 and LTB, involved in ectopic lymphoid structure development. Moreover, scRNAseq not only revealed that CD4+ T cells were the main producers of LTB but also identified a subset of clonally expanded CD8+ T cells, dominantly present in IR+ tumors, which secreted the T cell and dendritic cell (DC) attracting chemokine CCL4. Indeed, immune cell infiltration in IR+ tumors is stronger, highly coordinated, and has a distinct spatial phenotypical signature characterized by intratumoral microaggregates of CD8+CD103+ and CD4+ T cells with DCs. In contrast, the IR− TIME comprised spatial interactions between lymphocytes and various immunosuppressive myeloid cell populations. The impact of these chemokines on local immunity and clinical outcome was confirmed in an independent The Cancer Genome Atlas OPSCC cohort.ConclusionThe production of lymphoid cell attracting and organizing chemokines by tumor-specific T cells in IR+ tumors constitutes a positive feedback loop to sustain the formation of the DC–T-cell microaggregates and identifies patients with excellent survival after standard therapy.
AbstractList The composition of the tumor immune microenvironment (TIME) associated with good prognosis generally also predicts the success of immunotherapy, and both entail the presence of pre-existing tumor-specific T cells. Here, the blueprint of the TIME associated with such an ongoing tumor-specific T-cell response was dissected in a unique prospective oropharyngeal squamous cell carcinoma (OPSCC) cohort, in which tumor-specific tumor-infiltrating T cells were detected (immune responsiveness (IR+)) or not (lack of immune responsiveness (IR-)).BACKGROUNDThe composition of the tumor immune microenvironment (TIME) associated with good prognosis generally also predicts the success of immunotherapy, and both entail the presence of pre-existing tumor-specific T cells. Here, the blueprint of the TIME associated with such an ongoing tumor-specific T-cell response was dissected in a unique prospective oropharyngeal squamous cell carcinoma (OPSCC) cohort, in which tumor-specific tumor-infiltrating T cells were detected (immune responsiveness (IR+)) or not (lack of immune responsiveness (IR-)).A comprehensive multimodal, high-dimensional strategy was applied to dissect the TIME of treatment-naive IR+ and IR- OPSCC tissue, including bulk RNA sequencing (NanoString), imaging mass cytometry (Hyperion) for phenotyping and spatial interaction analyses of immune cells, and combined single-cell gene expression profiling and T-cell receptor (TCR) sequencing (single-cell RNA sequencing (scRNAseq)) to characterize the transcriptional states of clonally expanded tumor-infiltrating T cells.METHODSA comprehensive multimodal, high-dimensional strategy was applied to dissect the TIME of treatment-naive IR+ and IR- OPSCC tissue, including bulk RNA sequencing (NanoString), imaging mass cytometry (Hyperion) for phenotyping and spatial interaction analyses of immune cells, and combined single-cell gene expression profiling and T-cell receptor (TCR) sequencing (single-cell RNA sequencing (scRNAseq)) to characterize the transcriptional states of clonally expanded tumor-infiltrating T cells.IR+ patients had an excellent survival during >10 years follow-up. The tumors of IR+ patients expressed higher levels of genes strongly related to interferon gamma signaling, T-cell activation, TCR signaling, and mononuclear cell differentiation, as well as genes involved in several immune signaling pathways, than IR- patients. The top differently overexpressed genes included CXCL12 and LTB, involved in ectopic lymphoid structure development. Moreover, scRNAseq not only revealed that CD4+ T cells were the main producers of LTB but also identified a subset of clonally expanded CD8+ T cells, dominantly present in IR+ tumors, which secreted the T cell and dendritic cell (DC) attracting chemokine CCL4. Indeed, immune cell infiltration in IR+ tumors is stronger, highly coordinated, and has a distinct spatial phenotypical signature characterized by intratumoral microaggregates of CD8+CD103+ and CD4+ T cells with DCs. In contrast, the IR- TIME comprised spatial interactions between lymphocytes and various immunosuppressive myeloid cell populations. The impact of these chemokines on local immunity and clinical outcome was confirmed in an independent The Cancer Genome Atlas OPSCC cohort.RESULTSIR+ patients had an excellent survival during >10 years follow-up. The tumors of IR+ patients expressed higher levels of genes strongly related to interferon gamma signaling, T-cell activation, TCR signaling, and mononuclear cell differentiation, as well as genes involved in several immune signaling pathways, than IR- patients. The top differently overexpressed genes included CXCL12 and LTB, involved in ectopic lymphoid structure development. Moreover, scRNAseq not only revealed that CD4+ T cells were the main producers of LTB but also identified a subset of clonally expanded CD8+ T cells, dominantly present in IR+ tumors, which secreted the T cell and dendritic cell (DC) attracting chemokine CCL4. Indeed, immune cell infiltration in IR+ tumors is stronger, highly coordinated, and has a distinct spatial phenotypical signature characterized by intratumoral microaggregates of CD8+CD103+ and CD4+ T cells with DCs. In contrast, the IR- TIME comprised spatial interactions between lymphocytes and various immunosuppressive myeloid cell populations. The impact of these chemokines on local immunity and clinical outcome was confirmed in an independent The Cancer Genome Atlas OPSCC cohort.The production of lymphoid cell attracting and organizing chemokines by tumor-specific T cells in IR+ tumors constitutes a positive feedback loop to sustain the formation of the DC-T-cell microaggregates and identifies patients with excellent survival after standard therapy.CONCLUSIONThe production of lymphoid cell attracting and organizing chemokines by tumor-specific T cells in IR+ tumors constitutes a positive feedback loop to sustain the formation of the DC-T-cell microaggregates and identifies patients with excellent survival after standard therapy.
The composition of the tumor immune microenvironment (TIME) associated with good prognosis generally also predicts the success of immunotherapy, and both entail the presence of pre-existing tumor-specific T cells. Here, the blueprint of the TIME associated with such an ongoing tumor-specific T-cell response was dissected in a unique prospective oropharyngeal squamous cell carcinoma (OPSCC) cohort, in which tumor-specific tumor-infiltrating T cells were detected (immune responsiveness (IR )) or not (lack of immune responsiveness (IR )). A comprehensive multimodal, high-dimensional strategy was applied to dissect the TIME of treatment-naive IR and IR OPSCC tissue, including bulk RNA sequencing (NanoString), imaging mass cytometry (Hyperion) for phenotyping and spatial interaction analyses of immune cells, and combined single-cell gene expression profiling and T-cell receptor (TCR) sequencing (single-cell RNA sequencing (scRNAseq)) to characterize the transcriptional states of clonally expanded tumor-infiltrating T cells. IR patients had an excellent survival during >10 years follow-up. The tumors of IR patients expressed higher levels of genes strongly related to interferon gamma signaling, T-cell activation, TCR signaling, and mononuclear cell differentiation, as well as genes involved in several immune signaling pathways, than IR patients. The top differently overexpressed genes included and involved in ectopic lymphoid structure development. Moreover, scRNAseq not only revealed that CD4 T cells were the main producers of but also identified a subset of clonally expanded CD8 T cells, dominantly present in IR tumors, which secreted the T cell and dendritic cell (DC) attracting chemokine CCL4. Indeed, immune cell infiltration in IR tumors is stronger, highly coordinated, and has a distinct spatial phenotypical signature characterized by intratumoral microaggregates of CD8 CD103 and CD4 T cells with DCs. In contrast, the IR TIME comprised spatial interactions between lymphocytes and various immunosuppressive myeloid cell populations. The impact of these chemokines on local immunity and clinical outcome was confirmed in an independent The Cancer Genome Atlas OPSCC cohort. The production of lymphoid cell attracting and organizing chemokines by tumor-specific T cells in IR tumors constitutes a positive feedback loop to sustain the formation of the DC-T-cell microaggregates and identifies patients with excellent survival after standard therapy.
BackgroundThe composition of the tumor immune microenvironment (TIME) associated with good prognosis generally also predicts the success of immunotherapy, and both entail the presence of pre-existing tumor-specific T cells. Here, the blueprint of the TIME associated with such an ongoing tumor-specific T-cell response was dissected in a unique prospective oropharyngeal squamous cell carcinoma (OPSCC) cohort, in which tumor-specific tumor-infiltrating T cells were detected (immune responsiveness (IR+)) or not (lack of immune responsiveness (IR−)).MethodsA comprehensive multimodal, high-dimensional strategy was applied to dissect the TIME of treatment-naive IR+ and IR− OPSCC tissue, including bulk RNA sequencing (NanoString), imaging mass cytometry (Hyperion) for phenotyping and spatial interaction analyses of immune cells, and combined single-cell gene expression profiling and T-cell receptor (TCR) sequencing (single-cell RNA sequencing (scRNAseq)) to characterize the transcriptional states of clonally expanded tumor-infiltrating T cells.ResultsIR+ patients had an excellent survival during >10 years follow-up. The tumors of IR+ patients expressed higher levels of genes strongly related to interferon gamma signaling, T-cell activation, TCR signaling, and mononuclear cell differentiation, as well as genes involved in several immune signaling pathways, than IR− patients. The top differently overexpressed genes included CXCL12 and LTB, involved in ectopic lymphoid structure development. Moreover, scRNAseq not only revealed that CD4+ T cells were the main producers of LTB but also identified a subset of clonally expanded CD8+ T cells, dominantly present in IR+ tumors, which secreted the T cell and dendritic cell (DC) attracting chemokine CCL4. Indeed, immune cell infiltration in IR+ tumors is stronger, highly coordinated, and has a distinct spatial phenotypical signature characterized by intratumoral microaggregates of CD8+CD103+ and CD4+ T cells with DCs. In contrast, the IR− TIME comprised spatial interactions between lymphocytes and various immunosuppressive myeloid cell populations. The impact of these chemokines on local immunity and clinical outcome was confirmed in an independent The Cancer Genome Atlas OPSCC cohort.ConclusionThe production of lymphoid cell attracting and organizing chemokines by tumor-specific T cells in IR+ tumors constitutes a positive feedback loop to sustain the formation of the DC–T-cell microaggregates and identifies patients with excellent survival after standard therapy.
Background The composition of the tumor immune microenvironment (TIME) associated with good prognosis generally also predicts the success of immunotherapy, and both entail the presence of pre-existing tumor-specific T cells. Here, the blueprint of the TIME associated with such an ongoing tumor-specific T-cell response was dissected in a unique prospective oropharyngeal squamous cell carcinoma (OPSCC) cohort, in which tumor-specific tumor-infiltrating T cells were detected (immune responsiveness (IR+)) or not (lack of immune responsiveness (IR−)).Methods A comprehensive multimodal, high-dimensional strategy was applied to dissect the TIME of treatment-naive IR+ and IR− OPSCC tissue, including bulk RNA sequencing (NanoString), imaging mass cytometry (Hyperion) for phenotyping and spatial interaction analyses of immune cells, and combined single-cell gene expression profiling and T-cell receptor (TCR) sequencing (single-cell RNA sequencing (scRNAseq)) to characterize the transcriptional states of clonally expanded tumor-infiltrating T cells.Results IR+ patients had an excellent survival during >10 years follow-up. The tumors of IR+ patients expressed higher levels of genes strongly related to interferon gamma signaling, T-cell activation, TCR signaling, and mononuclear cell differentiation, as well as genes involved in several immune signaling pathways, than IR− patients. The top differently overexpressed genes included CXCL12 and LTB, involved in ectopic lymphoid structure development. Moreover, scRNAseq not only revealed that CD4+ T cells were the main producers of LTB but also identified a subset of clonally expanded CD8+ T cells, dominantly present in IR+ tumors, which secreted the T cell and dendritic cell (DC) attracting chemokine CCL4. Indeed, immune cell infiltration in IR+ tumors is stronger, highly coordinated, and has a distinct spatial phenotypical signature characterized by intratumoral microaggregates of CD8+CD103+ and CD4+ T cells with DCs. In contrast, the IR− TIME comprised spatial interactions between lymphocytes and various immunosuppressive myeloid cell populations. The impact of these chemokines on local immunity and clinical outcome was confirmed in an independent The Cancer Genome Atlas OPSCC cohort.Conclusion The production of lymphoid cell attracting and organizing chemokines by tumor-specific T cells in IR+ tumors constitutes a positive feedback loop to sustain the formation of the DC–T-cell microaggregates and identifies patients with excellent survival after standard therapy.
Author Sturm, Gregor
Ijsselsteijn, Marieke E
Welters, Marij J P
Finotello, Francesca
Abdulrahman, Ziena
Somarakis, Antonios
van Egmond, Sylvia L
de Miranda, Noel F C C
Charoentong, Pornpimol
Höllt, Thomas
Mustafa, Dana A M
van der Burg, Sjoerd H
Trajanoski, Zlatko
Santegoets, Saskia J
AuthorAffiliation 6 Medical University of Innsbruck , Innsbruck , Austria
7 Otolaryngology , Leiden University Medical Center , Leiden , The Netherlands
2 Biocenter, Institute of Bioinformatics , Medical University of Innsbruck , Innsbruck , Austria
3 Medical Oncology and National Center for Tumor diseases , University Hospital Heidelberg, German Cancer Research Center , Heidelberg , Germany
4 Pathology , Leiden University Medical Center , Leiden , The Netherlands
8 Pathology, Tumor Immuno-Pathology Laboratory , Leiden University Medical Center , Leiden , The Netherlands
1 Medical Oncology, Oncode Institute , Leiden University Medical Center , Leiden , The Netherlands
5 Radiology , Leiden University Medical Center , Leiden , The Netherlands
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– name: 3 Medical Oncology and National Center for Tumor diseases , University Hospital Heidelberg, German Cancer Research Center , Heidelberg , Germany
– name: 7 Otolaryngology , Leiden University Medical Center , Leiden , The Netherlands
– name: 1 Medical Oncology, Oncode Institute , Leiden University Medical Center , Leiden , The Netherlands
– name: 2 Biocenter, Institute of Bioinformatics , Medical University of Innsbruck , Innsbruck , Austria
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  surname: Abdulrahman
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  givenname: Saskia J
  orcidid: 0000-0002-2874-4402
  surname: Santegoets
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  fullname: Höllt, Thomas
  organization: Radiology, Leiden University Medical Center, Leiden, The Netherlands
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  orcidid: 0000-0003-0712-4658
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  organization: Medical University of Innsbruck, Innsbruck, Austria
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/35217577$$D View this record in MEDLINE/PubMed
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Issue 2
Keywords immunotherapy
tumor microenvironment
Language English
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Snippet BackgroundThe composition of the tumor immune microenvironment (TIME) associated with good prognosis generally also predicts the success of immunotherapy, and...
The composition of the tumor immune microenvironment (TIME) associated with good prognosis generally also predicts the success of immunotherapy, and both...
Background The composition of the tumor immune microenvironment (TIME) associated with good prognosis generally also predicts the success of immunotherapy, and...
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StartPage e004346
SubjectTerms Antigens
Basic Tumor Immunology
Cancer
Cancer therapies
Chemokines - metabolism
Cytokines
Female
Gene expression
Head & neck cancer
Human papillomavirus
Humans
Immunotherapy
Lymphocytes
Male
Medical prognosis
Monitoring, Immunologic - methods
Patients
Quality control
Software
Squamous cell carcinoma
Surgery
T-Lymphocytes - metabolism
Throat cancer
tumor microenvironment
Tumor Microenvironment - immunology
Tumor necrosis factor-TNF
Tumors
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Title Tumor-specific T cells support chemokine-driven spatial organization of intratumoral immune microaggregates needed for long survival
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