Functional Heterogeneity of CD4+ Tumor-Infiltrating Lymphocytes With a Resident Memory Phenotype in NSCLC
Open accessAbstract
Resident memory T cells (TRM) inhabit peripheral tissues and are critical for protection against localized infections. Recently, it has become evident that CD103+ TRM are not only important in combating secondary infections, but also for the elimination of tumor cells. In several solid cancers, intratumoral CD103+CD8+ tumor infiltrating lymphocytes (TILs), with TRM properties, are a positive prognostic marker. To better understand the role of TRM in tumors, we performed a detailed characterization of CD8+ and CD4+ TIL phenotype and functional properties in non-small cell lung cancer (NSCLC). Frequencies of CD8+ and CD4+ T cell infiltrates in tumors were comparable, but we observed a sharp contrast in TRM ratios compared to surrounding lung tissue. The majority of both CD4+ and CD8+ TILs expressed CD69 and a subset also expressed CD103, both hallmarks of TRM. While CD103+CD8+ T cells were enriched in tumors, CD103+CD4+ T cell frequencies were decreased compared to surrounding lung tissue. Furthermore, CD103+CD4+ and CD103+CD8+ TILs showed multiple characteristics of TRM, such as elevated expression of CXCR6 and CD49a, and decreased expression of T-bet and Eomes. In line with the immunomodulatory role of the tumor microenvironment, CD8+ and CD4+ TILs expressed high levels of inhibitory receptors 2B4, CTLA-4, and PD-1, with the highest levels found on CD103+ TILs. Strikingly, CD103+CD4+ TILs were the most potent producers of TNF- and IFN-, while other TIL subsets lacked such cytokine production. Whereas CD103+CD4+PD-1low TILs produced the most effector cytokines, CD103+CD4+PD-1++ and CD69+CD4+PD-1++ TILs produced CXCL13. Furthermore, a large proportion of TILs expressed co-stimulatory receptors CD27 and CD28, unlike lung TRM, suggesting a less differentiated phenotype. Agonistic triggering of these receptors improved cytokine production of CD103+CD4+ and CD69+CD8+ TILs. Our findings thus provide a rationale to target CD103+CD4+ TILs and add co-stimulation to current therapies to improve the efficacy of immunotherapies and cancer vaccines.
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A proportion of PD-1++ TILs with a Trm phenotype also express CXCL13, the ligand of CXCR5.
“A proportion of PD-1++ TILs with a Trm phenotype also express CXCL13, the ligand of CXCR5 [273-275].”
From Guidelines for the use of flow cytometry and cell sorting in immunological studies (third edition) (2021) · cites this paper as [273]
A subset of TILs in tumors of NSCLC shares the phenotype of Trm in adjacent lung tissue (expression of CD103, CD69, CXCR6, CD49a).
“A subset of TILs in tumors of NSCLC shares the phenotype of Trm in adjacent lung tissue (expression of CD103, CD69, CXCR6, CD49a) [272, 273].”
From Guidelines for the use of flow cytometry and cell sorting in immunological studies (third edition) (2021) · cites this paper as [273]
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- Authors
- Oja, A. E., Piet, B., van der Zwan, D., Blaauwgeers, H., Mensink, M., de Kivit, S., Borst, J., Nolte, M. A., van Lier, R. A. W., Stark, R., & Hombrink, P.
- Affiliations
- Sanquin (NL)
- OLVG (NL)
- The Netherlands Cancer Institute (NL)
- Corresponding author
- Oja, Anna E.
- Hombrink, Pleun
- ORCID
- Venue
- Frontiers in Immunology
- Publisher
- Frontiers Media SA
- Published
- 2018-11-16
- Volume
- 9
- Pages
- 2654-2654
- ISSN
- 1664-3224 (ISSN-L)
- PMC
- PMC6250821
- OpenAlex
- W2901131610
- Cited by
- 130
- References
- 100
- Citations by year
- 2026: 12 · 2025: 15 · 2024: 15 · 2023: 13 · 2022: 25 · 2021: 22 · 2020: 23 · 2019: 5
- FWCI
- 5.37
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Frontiers in Immunology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Pure Amsterdam UMC (submittedVersion, cc-by)
- Radboud Repository (Radboud University) (submittedVersion)
- Radboud Repository (Radboud University) (submittedVersion, other-oa)
- Funders
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Keywords
- tissue-resident memory T cells, CD4+ T cells, CD8+ T cells, tumor-infiltrating lymphocytes, non-small cell lung cancer, CD103, CD69, CXCR6, CD49a, PD-1, CTLA-4, 2B4, inhibitory receptors, T cell differentiation, costimulatory receptors, CXCL13, TNF-α, interferon-gamma, tumor microenvironment, T cell heterogeneity, adoptive T cell therapy
- MeSH terms
- Receptors, CXCR6, Aged, Carcinoma, Non-Small-Cell Lung, Female, Humans, Immunologic Memory, Lung, Lung Neoplasms, Male, Middle Aged, Phenotype, Prognosis, CD4-Positive T-Lymphocytes, Antigens, CD, Cytokines, Lymphocytes, Tumor-Infiltrating, CD8-Positive T-Lymphocytes, Integrin alpha Chains, Integrin alpha1, Granzymes, Tumor Microenvironment, Programmed Cell Death 1 Receptor
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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