Comparative analysis of immune infiltrates in head and neck cancers across anatomical sites
BackgroundThe response rate to immune checkpoint inhibitors targeting programmed cell death 1 (PD-1) receptor is 13%–18% for patients with recurrent or metastatic head and neck squamous cell carcinoma (HNSCC). Detailed understanding of the tumor immune microenvironment (TIME) is crucial in order to...
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| Published in: | Journal for immunotherapy of cancer Vol. 12; no. 1; p. e007573 |
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11.01.2024
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| Abstract | BackgroundThe response rate to immune checkpoint inhibitors targeting programmed cell death 1 (PD-1) receptor is 13%–18% for patients with recurrent or metastatic head and neck squamous cell carcinoma (HNSCC). Detailed understanding of the tumor immune microenvironment (TIME) is crucial in order to explain and improve this response rate. HNSCCs arise at various anatomical locations including the oral cavity, hypopharynx, larynx and oropharynx. Studies directly comparing immune infiltration between anatomical sites are scarce. Since the distinct locations could drive deviating microenvironments, we questioned whether the immune composition varies across these HNSCC sites.MethodsHere, we characterized the TIME of 76 fresh tumor specimens using flow cytometry and performed single-cell RNA-sequencing on nine head and neck tumor samples.ResultsWe found major differences in the composition of the TIME between patients. When comparing anatomical sites: tumors originating from the oral cavity had higher T cell infiltrates than tumors from other anatomical sites. The percentage of tumor-infiltrating T-lymphocytes positive for the immune checkpoint PD-1 varied considerably between patients, with the highest fraction of PD-1+ T cells found in larynx squamous cell carcinomas (SCCs). While we had hypothesized that the anatomical sites of tumor origin would drive sample clustering, our data showed that the type of TIME was more dominant and was particularly driven by the fraction of T cells positive for PD-1. Moreover, a high proportion of PD-1+ CD8+ T cells associated with an improved overall survival. Using single-cell RNA-sequencing, we observed that PD-1 expression was highest in the CD8-ENTPD1 tissue resident memory T cell/exhausted T cell and CD4-CXCL13 type 1 T helper cell clusters.ConclusionsWe found that oral cavity SCCs had the highest frequencies of T cells. We also observed considerable interpatient heterogeneity for PD-1 on T cells, with noticeably higher frequencies of PD-1+ CD4+ T helper cells in larynx SCCs. Within the entire cohort, a higher fraction of CD8+ T cells positive for PD-1 was linked to improved overall survival. Whether the fraction of PD-1+ T cells within the TIME enables immune checkpoint inhibitor response prediction for patients with head and neck cancer remains to be determined. |
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| AbstractList | BackgroundThe response rate to immune checkpoint inhibitors targeting programmed cell death 1 (PD-1) receptor is 13%–18% for patients with recurrent or metastatic head and neck squamous cell carcinoma (HNSCC). Detailed understanding of the tumor immune microenvironment (TIME) is crucial in order to explain and improve this response rate. HNSCCs arise at various anatomical locations including the oral cavity, hypopharynx, larynx and oropharynx. Studies directly comparing immune infiltration between anatomical sites are scarce. Since the distinct locations could drive deviating microenvironments, we questioned whether the immune composition varies across these HNSCC sites.MethodsHere, we characterized the TIME of 76 fresh tumor specimens using flow cytometry and performed single-cell RNA-sequencing on nine head and neck tumor samples.ResultsWe found major differences in the composition of the TIME between patients. When comparing anatomical sites: tumors originating from the oral cavity had higher T cell infiltrates than tumors from other anatomical sites. The percentage of tumor-infiltrating T-lymphocytes positive for the immune checkpoint PD-1 varied considerably between patients, with the highest fraction of PD-1+ T cells found in larynx squamous cell carcinomas (SCCs). While we had hypothesized that the anatomical sites of tumor origin would drive sample clustering, our data showed that the type of TIME was more dominant and was particularly driven by the fraction of T cells positive for PD-1. Moreover, a high proportion of PD-1+ CD8+ T cells associated with an improved overall survival. Using single-cell RNA-sequencing, we observed that PD-1 expression was highest in the CD8-ENTPD1 tissue resident memory T cell/exhausted T cell and CD4-CXCL13 type 1 T helper cell clusters.ConclusionsWe found that oral cavity SCCs had the highest frequencies of T cells. We also observed considerable interpatient heterogeneity for PD-1 on T cells, with noticeably higher frequencies of PD-1+ CD4+ T helper cells in larynx SCCs. Within the entire cohort, a higher fraction of CD8+ T cells positive for PD-1 was linked to improved overall survival. Whether the fraction of PD-1+ T cells within the TIME enables immune checkpoint inhibitor response prediction for patients with head and neck cancer remains to be determined. Background The response rate to immune checkpoint inhibitors targeting programmed cell death 1 (PD-1) receptor is 13%–18% for patients with recurrent or metastatic head and neck squamous cell carcinoma (HNSCC). Detailed understanding of the tumor immune microenvironment (TIME) is crucial in order to explain and improve this response rate. HNSCCs arise at various anatomical locations including the oral cavity, hypopharynx, larynx and oropharynx. Studies directly comparing immune infiltration between anatomical sites are scarce. Since the distinct locations could drive deviating microenvironments, we questioned whether the immune composition varies across these HNSCC sites.Methods Here, we characterized the TIME of 76 fresh tumor specimens using flow cytometry and performed single-cell RNA-sequencing on nine head and neck tumor samples.Results We found major differences in the composition of the TIME between patients. When comparing anatomical sites: tumors originating from the oral cavity had higher T cell infiltrates than tumors from other anatomical sites. The percentage of tumor-infiltrating T-lymphocytes positive for the immune checkpoint PD-1 varied considerably between patients, with the highest fraction of PD-1+ T cells found in larynx squamous cell carcinomas (SCCs). While we had hypothesized that the anatomical sites of tumor origin would drive sample clustering, our data showed that the type of TIME was more dominant and was particularly driven by the fraction of T cells positive for PD-1. Moreover, a high proportion of PD-1+ CD8+ T cells associated with an improved overall survival. Using single-cell RNA-sequencing, we observed that PD-1 expression was highest in the CD8-ENTPD1 tissue resident memory T cell/exhausted T cell and CD4-CXCL13 type 1 T helper cell clusters.Conclusions We found that oral cavity SCCs had the highest frequencies of T cells. We also observed considerable interpatient heterogeneity for PD-1 on T cells, with noticeably higher frequencies of PD-1+ CD4+ T helper cells in larynx SCCs. Within the entire cohort, a higher fraction of CD8+ T cells positive for PD-1 was linked to improved overall survival. Whether the fraction of PD-1+ T cells within the TIME enables immune checkpoint inhibitor response prediction for patients with head and neck cancer remains to be determined. The response rate to immune checkpoint inhibitors targeting programmed cell death 1 (PD-1) receptor is 13%-18% for patients with recurrent or metastatic head and neck squamous cell carcinoma (HNSCC). Detailed understanding of the tumor immune microenvironment (TIME) is crucial in order to explain and improve this response rate. HNSCCs arise at various anatomical locations including the oral cavity, hypopharynx, larynx and oropharynx. Studies directly comparing immune infiltration between anatomical sites are scarce. Since the distinct locations could drive deviating microenvironments, we questioned whether the immune composition varies across these HNSCC sites.BACKGROUNDThe response rate to immune checkpoint inhibitors targeting programmed cell death 1 (PD-1) receptor is 13%-18% for patients with recurrent or metastatic head and neck squamous cell carcinoma (HNSCC). Detailed understanding of the tumor immune microenvironment (TIME) is crucial in order to explain and improve this response rate. HNSCCs arise at various anatomical locations including the oral cavity, hypopharynx, larynx and oropharynx. Studies directly comparing immune infiltration between anatomical sites are scarce. Since the distinct locations could drive deviating microenvironments, we questioned whether the immune composition varies across these HNSCC sites.Here, we characterized the TIME of 76 fresh tumor specimens using flow cytometry and performed single-cell RNA-sequencing on nine head and neck tumor samples.METHODSHere, we characterized the TIME of 76 fresh tumor specimens using flow cytometry and performed single-cell RNA-sequencing on nine head and neck tumor samples.We found major differences in the composition of the TIME between patients. When comparing anatomical sites: tumors originating from the oral cavity had higher T cell infiltrates than tumors from other anatomical sites. The percentage of tumor-infiltrating T-lymphocytes positive for the immune checkpoint PD-1 varied considerably between patients, with the highest fraction of PD-1+ T cells found in larynx squamous cell carcinomas (SCCs). While we had hypothesized that the anatomical sites of tumor origin would drive sample clustering, our data showed that the type of TIME was more dominant and was particularly driven by the fraction of T cells positive for PD-1. Moreover, a high proportion of PD-1+ CD8+ T cells associated with an improved overall survival. Using single-cell RNA-sequencing, we observed that PD-1 expression was highest in the CD8-ENTPD1 tissue resident memory T cell/exhausted T cell and CD4-CXCL13 type 1 T helper cell clusters.RESULTSWe found major differences in the composition of the TIME between patients. When comparing anatomical sites: tumors originating from the oral cavity had higher T cell infiltrates than tumors from other anatomical sites. The percentage of tumor-infiltrating T-lymphocytes positive for the immune checkpoint PD-1 varied considerably between patients, with the highest fraction of PD-1+ T cells found in larynx squamous cell carcinomas (SCCs). While we had hypothesized that the anatomical sites of tumor origin would drive sample clustering, our data showed that the type of TIME was more dominant and was particularly driven by the fraction of T cells positive for PD-1. Moreover, a high proportion of PD-1+ CD8+ T cells associated with an improved overall survival. Using single-cell RNA-sequencing, we observed that PD-1 expression was highest in the CD8-ENTPD1 tissue resident memory T cell/exhausted T cell and CD4-CXCL13 type 1 T helper cell clusters.We found that oral cavity SCCs had the highest frequencies of T cells. We also observed considerable interpatient heterogeneity for PD-1 on T cells, with noticeably higher frequencies of PD-1+ CD4+ T helper cells in larynx SCCs. Within the entire cohort, a higher fraction of CD8+ T cells positive for PD-1 was linked to improved overall survival. Whether the fraction of PD-1+ T cells within the TIME enables immune checkpoint inhibitor response prediction for patients with head and neck cancer remains to be determined.CONCLUSIONSWe found that oral cavity SCCs had the highest frequencies of T cells. We also observed considerable interpatient heterogeneity for PD-1 on T cells, with noticeably higher frequencies of PD-1+ CD4+ T helper cells in larynx SCCs. Within the entire cohort, a higher fraction of CD8+ T cells positive for PD-1 was linked to improved overall survival. Whether the fraction of PD-1+ T cells within the TIME enables immune checkpoint inhibitor response prediction for patients with head and neck cancer remains to be determined. The response rate to immune checkpoint inhibitors targeting programmed cell death 1 (PD-1) receptor is 13%-18% for patients with recurrent or metastatic head and neck squamous cell carcinoma (HNSCC). Detailed understanding of the tumor immune microenvironment (TIME) is crucial in order to explain and improve this response rate. HNSCCs arise at various anatomical locations including the oral cavity, hypopharynx, larynx and oropharynx. Studies directly comparing immune infiltration between anatomical sites are scarce. Since the distinct locations could drive deviating microenvironments, we questioned whether the immune composition varies across these HNSCC sites. Here, we characterized the TIME of 76 fresh tumor specimens using flow cytometry and performed single-cell RNA-sequencing on nine head and neck tumor samples. We found major differences in the composition of the TIME between patients. When comparing anatomical sites: tumors originating from the oral cavity had higher T cell infiltrates than tumors from other anatomical sites. The percentage of tumor-infiltrating T-lymphocytes positive for the immune checkpoint PD-1 varied considerably between patients, with the highest fraction of PD-1+ T cells found in larynx squamous cell carcinomas (SCCs). While we had hypothesized that the anatomical sites of tumor origin would drive sample clustering, our data showed that the type of TIME was more dominant and was particularly driven by the fraction of T cells positive for PD-1. Moreover, a high proportion of PD-1+ CD8+ T cells associated with an improved overall survival. Using single-cell RNA-sequencing, we observed that PD-1 expression was highest in the CD8-ENTPD1 tissue resident memory T cell/exhausted T cell and CD4-CXCL13 type 1 T helper cell clusters. We found that oral cavity SCCs had the highest frequencies of T cells. We also observed considerable interpatient heterogeneity for PD-1 on T cells, with noticeably higher frequencies of PD-1+ CD4+ T helper cells in larynx SCCs. Within the entire cohort, a higher fraction of CD8+ T cells positive for PD-1 was linked to improved overall survival. Whether the fraction of PD-1+ T cells within the TIME enables immune checkpoint inhibitor response prediction for patients with head and neck cancer remains to be determined. |
| Author | Fass, Joseph N Ganzevles, Sonja H Leemans, C René van de Ven, Rieneke Ke, Changlin Brink, Arjen Fox, Bernard A Muijlwijk, Tara Rajamanickam, Venkatesh Brakenhoff, Ruud H Koguchi, Yoshinobu Poell, Jos B Nijenhuis, Dennis N L M |
| AuthorAffiliation | 2 Cancer Biology and Immunology , Cancer Center Amsterdam , Amsterdam , The Netherlands 1 Department of Otolaryngology/Head and Neck Surgery , Amsterdam UMC Location VUmc , Amsterdam , The Netherlands 3 Cancer Immunology , Amsterdam Institute for Infection and Immunity , Amsterdam , The Netherlands 4 Providence Cancer Institute , Earle A Chiles Research Institute , Portland , Oregon , USA |
| AuthorAffiliation_xml | – name: 4 Providence Cancer Institute , Earle A Chiles Research Institute , Portland , Oregon , USA – name: 3 Cancer Immunology , Amsterdam Institute for Infection and Immunity , Amsterdam , The Netherlands – name: 1 Department of Otolaryngology/Head and Neck Surgery , Amsterdam UMC Location VUmc , Amsterdam , The Netherlands – name: 2 Cancer Biology and Immunology , Cancer Center Amsterdam , Amsterdam , The Netherlands |
| Author_xml | – sequence: 1 givenname: Tara orcidid: 0000-0003-3827-5694 surname: Muijlwijk fullname: Muijlwijk, Tara organization: Cancer Immunology, Amsterdam Institute for Infection and Immunity, Amsterdam, The Netherlands – sequence: 2 givenname: Dennis N L M surname: Nijenhuis fullname: Nijenhuis, Dennis N L M organization: Cancer Immunology, Amsterdam Institute for Infection and Immunity, Amsterdam, The Netherlands – sequence: 3 givenname: Sonja H surname: Ganzevles fullname: Ganzevles, Sonja H organization: Cancer Immunology, Amsterdam Institute for Infection and Immunity, Amsterdam, The Netherlands – sequence: 4 givenname: Arjen surname: Brink fullname: Brink, Arjen organization: Cancer Biology and Immunology, Cancer Center Amsterdam, Amsterdam, The Netherlands – sequence: 5 givenname: Changlin surname: Ke fullname: Ke, Changlin organization: Cancer Biology and Immunology, Cancer Center Amsterdam, Amsterdam, The Netherlands – sequence: 6 givenname: Joseph N surname: Fass fullname: Fass, Joseph N organization: Providence Cancer Institute, Earle A Chiles Research Institute, Portland, Oregon, USA – sequence: 7 givenname: Venkatesh surname: Rajamanickam fullname: Rajamanickam, Venkatesh organization: Providence Cancer Institute, Earle A Chiles Research Institute, Portland, Oregon, USA – sequence: 8 givenname: C René surname: Leemans fullname: Leemans, C René organization: Cancer Biology and Immunology, Cancer Center Amsterdam, Amsterdam, The Netherlands – sequence: 9 givenname: Yoshinobu surname: Koguchi fullname: Koguchi, Yoshinobu organization: Providence Cancer Institute, Earle A Chiles Research Institute, Portland, Oregon, USA – sequence: 10 givenname: Bernard A orcidid: 0000-0002-4452-5947 surname: Fox fullname: Fox, Bernard A organization: Providence Cancer Institute, Earle A Chiles Research Institute, Portland, Oregon, USA – sequence: 11 givenname: Jos B surname: Poell fullname: Poell, Jos B organization: Cancer Biology and Immunology, Cancer Center Amsterdam, Amsterdam, The Netherlands – sequence: 12 givenname: Ruud H surname: Brakenhoff fullname: Brakenhoff, Ruud H organization: Cancer Biology and Immunology, Cancer Center Amsterdam, Amsterdam, The Netherlands – sequence: 13 givenname: Rieneke orcidid: 0000-0002-4230-8383 surname: van de Ven fullname: van de Ven, Rieneke email: r.vandeven@amsterdamumc.nl organization: Cancer Immunology, Amsterdam Institute for Infection and Immunity, Amsterdam, The Netherlands |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/38212122$$D View this record in MEDLINE/PubMed |
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| Keywords | Tumor Microenvironment Programmed Cell Death 1 Receptor Lymphocytes, Tumor-Infiltrating T-Lymphocytes Head and Neck Neoplasms |
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| 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 | 2024 |
| 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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2025100303050253000_12.1.e007573.35 doi: 10.1172/JCI87324 – volume: 12 year: 2021 ident: 2025100303050253000_12.1.e007573.30 article-title: Immunomodulation of T helper cells by tumor microenvironment in oral cancer is associated with CCR8 expression and rapid membrane vitamin D signaling pathway publication-title: Front Immunol doi: 10.3389/fimmu.2021.643298 – ident: 2025100303050253000_12.1.e007573.39 doi: 10.1016/j.jtho.2017.11.132 – volume: 40 start-page: 479 year: 2022 ident: 2025100303050253000_12.1.e007573.47 article-title: A phenotypic signature that identifies neoantigen-reactive T cells in fresh human lung cancers publication-title: Cancer Cell doi: 10.1016/j.ccell.2022.03.012 – volume: 28 start-page: 1345 year: 2022 ident: 2025100303050253000_12.1.e007573.8 article-title: Phase II clinical trial of neoadjuvant and adjuvant pembrolizumab in resectable local-regionally advanced head and neck squamous cell carcinoma publication-title: Clin Cancer Res doi: 10.1158/1078-0432.CCR-21-3351 |
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| Snippet | BackgroundThe response rate to immune checkpoint inhibitors targeting programmed cell death 1 (PD-1) receptor is 13%–18% for patients with recurrent or... The response rate to immune checkpoint inhibitors targeting programmed cell death 1 (PD-1) receptor is 13%-18% for patients with recurrent or metastatic head... Background The response rate to immune checkpoint inhibitors targeting programmed cell death 1 (PD-1) receptor is 13%–18% for patients with recurrent or... |
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| SubjectTerms | Antibodies Basic Tumor Immunology Cancer therapies Carcinogens Cell death Datasets Flow cytometry Genomes Head & neck cancer Head and Neck Neoplasms Human papillomavirus Immune checkpoint inhibitors Immunology Laryngeal cancer Larynx Lymphocytes Lymphocytes, Tumor-Infiltrating Medical prognosis Metastasis Patients Programmed Cell Death 1 Receptor Squamous cell carcinoma T-Lymphocytes Tumor Microenvironment Tumors |
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| Title | Comparative analysis of immune infiltrates in head and neck cancers across anatomical sites |
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