Markers of T Cell Infiltration and Function Associate with Favorable Outcome in Vascularized High-Grade Serous Ovarian Carcinoma
Open accessAbstract
BACKGROUND: When T cells infiltrate the tumor environment they encounter a myriad of metabolic stressors including hypoxia. Overcoming the limitations imposed by an inadequate tumor vasculature that contributes to these stressors may be a crucial step to immune cells mounting an effective anti-tumor response. We sought to determine whether the functional capacity of tumor infiltrating lymphocytes (TIL) could be influenced by the tumor vasculature and correlated this with survival in patients with ovarian cancer. METHODOLOGY AND PRINCIPAL FINDINGS: In 196 high-grade serous ovarian tumors, we confirmed that the tumor vascularity as measured by the marker CD31 was associated with improved patient disease-specific survival. We also found that tumors positive for markers of TIL (CD8, CD4 and forkhead box P3 (FoxP3)) and T cell function (granzyme B and T-cell restricted intracellular antigen-1 (TIA-1)) correlated significantly with elevated vascularity. In vitro, hypoxic CD8 T cells showed reduced cytolytic activity, secreted less effector cytokines and upregulated autophagy. Survival analysis revealed that patients had a significant improvement in disease-specific survival when FoxP3 expressing cells were present in CD31-high tumors compared to patients with FoxP3 expressing cells in CD31-low tumors [HR: 2.314 (95% CI 1.049-5.106); p = 0.0377]. Patients with high vascular endothelial growth factor (VEGF) expressing tumors containing granzyme B positive cells had improved survival compared to patients with granzyme B positive cells in VEGF-low tumors [HR: 2.522 (95% CI 1.097-5.799); p = 0.0294]. SIGNIFICANCE: Overall, this data provides a rationale for developing strategies aimed at improving the adaptability and function of TIL to hypoxic tumor conditions.
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Considerable evidence in mouse models has shown that hypoxia promotes tumor escape from immune surveillance and immunotherapy.
“Considerable evidence in mouse models has shown that hypoxia promotes tumor escape from immune surveillance and immunotherapy13–19.”
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- Authors
- Townsend, K. N., Spowart, J. E., Huwait, H., Eshragh, S., West, N. R., Elrick, M. A., Kalloger, S. E., Anglesio, M., Watson, P. H., Huntsman, D. G., & Lum, J. J.
- Affiliations
- BC Cancer Agency (CA)
- Vancouver General Hospital (CA)
- University of British Columbia (CA)
- Corresponding author
- Lum, Julian J.
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2013-12-23
- Volume
- 8
- Issue
- 12
- Pages
- e82406
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3871161
- OpenAlex
- W1971998672
- Cited by
- 29
- References
- 46
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 3 · 2023: 1 · 2022: 2 · 2021: 1 · 2020: 2 · 2019: 1 · 2018: 2 · 2017: 4 · 2016: 1 · 2015: 4 · 2014: 4
- FWCI
- 3.63
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- University of Victoria
- Ovarian Cancer Canada
- LOEWE Zentrum AdRIA
- Canadian Institutes of Health Research (MSH191375, MOP201945)
- BC Cancer Agency
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Ovarian cancer diagnosis and treatment
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Health Sciences › Medicine › Psychiatry and Mental health › Cancer, Stress, Anesthesia, and Immune Response
- Keywords
- high-grade serous ovarian cancer, tumor-infiltrating lymphocytes, tumor vasculature, tumor vascularity, CD31, hypoxia, T cell function, granzyme B, TIA-1, Foxp3, regulatory T cells, vascular endothelial growth factor, disease-specific survival, autophagy, cytotoxicity
- MeSH terms
- T-Cell Intracellular Antigen-1, Adult, Aged, Aged, 80 and over, Animals, Autophagy, Female, Follow-Up Studies, Humans, Middle Aged, Ovarian Neoplasms, Biomarkers, Tumor, Cell Hypoxia, Survival Analysis, Lymphocytes, Tumor-Infiltrating, Treatment Outcome, Cystadenocarcinoma, Serous, CD8-Positive T-Lymphocytes, Platelet Endothelial Cell Adhesion Molecule-1, Poly(A)-Binding Proteins, Mice, Granzymes, Neoplasm Grading
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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