Cooperation between Constitutive and Inducible Chemokines Enables T Cell Engraftment and Immune Attack in Solid Tumors
Open accessAbstract
We investigated the role of chemokines in regulating T cell accumulation in solid tumors. CCL5 and CXCL9 overexpression was associated with CD8+ T cell infiltration in solid tumors. T cell infiltration required tumor cell-derived CCL5 and was amplified by IFN-γ-inducible, myeloid cell-secreted CXCL9. CCL5 and CXCL9 coexpression revealed immunoreactive tumors with prolonged survival and response to checkpoint blockade. Loss of CCL5 expression in human tumors was associated with epigenetic silencing through DNA methylation. Reduction of CCL5 expression caused tumor-infiltrating lymphocyte (TIL) desertification, whereas forced CCL5 expression prevented Cxcl9 expression and TILs loss, and attenuated tumor growth in mice through IFN-γ. The cooperation between tumor-derived CCL5 and IFN-γ-inducible CXCR3 ligands secreted by myeloid cells is key for orchestrating T cell infiltration in immunoreactive and immunoresponsive tumors.
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CXCL10 and CCL5 are dominant mediators for recruitment of CXCR3+ and CCR5+ tumor-specific T lymphocytes into tumors, and their intratumoral expression correlates with favorable clinical outcomes in melanoma.
“These chemokines have been identified as the dominant mediators for the recruitment of CXCR3+ and CCR5+ tumor-specific T lymphocytes into the tumors and their intratumoral expression correlated with favorable clinical outcomes in patients with melanoma30–32.”
From Epigenetic state determines the in vivo efficacy of STING agonist therapy (2023) · cites this paper as [32]
The Introduction links CXCL10 and CCL5 to T-cell infiltration in melanoma and describes the importance of CXCR3 and CCR5 on tumor-infiltrating lymphocytes. However, the Results identify CCL5 and CXCL9—not CXCL10—as the key pair associated with T-cell engraftment and longer survival in melanoma. Section labels are available in our copy, but page numbers are not. (LLM, conf=0.88)
Experimental — accuracy not yet measuredTogether with CXCL9, CXCL10 is a dominant chemokine for the recruitment of tumor-specific CD8+ T cells into tumors.
“Together with CXCL9, another CXCR3-binding chemokine, CXCL10 is a dominant chemokine for the recruitment of tumor-specific CD8+ T cells into the tumors31,32.”
From Epigenetic state determines the in vivo efficacy of STING agonist therapy (2023) · cites this paper as [32]
The Results and Discussion link CXCL9 to CD8+ T-cell infiltration and T-cell recruitment. The Discussion says CXCL10 may have a complementary role, but that CXCL10 expression does not correlate closely with CD8+ infiltration and may not translate to effective infiltration. The paper therefore does not support calling CXCL10 a dominant recruitment chemokine alongside CXCL9. Page numbers are unavailable in our copy. (LLM, conf=0.86)
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- Authors
- Dangaj, D., Bruand, M., Grimm, A. J., Ronet, C., Barras, D., Duttagupta, P. A., Lanitis, E., Duraiswamy, J., Tanyi, J. L., Benencia, F., Conejo-Garcia, J., Ramay, H. R., Montone, K. T., Powell, D. J., Gimotty, P. A., Facciabene, A., Jackson, D. G., Weber, J. S., Rodig, S. J., Hodi, S. F., Kandalaft, L. E., Irving, M., Zhang, L., Foukas, P., Rusakiewicz, S., Delorenzi, M., & Coukos, G.
- Affiliations
- Ludwig Cancer Research (CH)
- SIB Swiss Institute of Bioinformatics (CH)
- University of Chicago (US)
- Center for Biologics Evaluation and Research (US)
- University of Pennsylvania (US)
- Moffitt Cancer Center (US)
- Bristol-Myers Squibb (United States) (US)
- NYU Langone’s Laura and Isaac Perlmutter Cancer Center (US)
- Brigham and Women's Hospital (US)
- Dana-Farber Cancer Institute (US)
- National and Kapodistrian University of Athens (GR)
- Corresponding author
- Coukos, George
- ORCID
- Bruand, Marine
- Grimm, Alizée J.
- Ronet, Catherine
- Barras, David
- Lanitis, Evripidis
- Duraiswamy, Jaikumar
- Tanyi, Janos L.
- Conejo-Garcia, Jose
- Ramay, Hena R.
- Montone, Kathleen T.
- Powell, Daniel J.
- Gimotty, Phyllis A.
- Facciabene, Andrea
- Jackson, Donald G.
- Weber, Jeffrey S.
- Rodig, Scott J.
- Kandalaft, Lana E.
- Irving, Melita
- Foukas, Periklis
- Rusakiewicz, Sylvie
- Delorenzi, Mauro
- Coukos, George
- Venue
- Cancer Cell
- Publisher
- Elsevier BV
- Published
- 2019-06
- Volume
- 35
- Issue
- 6
- Pages
- 885-900.e10
- ISSN
- 1535-6108 (ISSN-L)
- PMC
- PMC6961655
- OpenAlex
- W2949498852
- Cited by
- 875
- References
- 11
- Citations by year
- 2026: 97 · 2025: 123 · 2024: 162 · 2023: 141 · 2022: 154 · 2021: 122 · 2020: 67 · 2019: 9
- FWCI
- 38.35
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cancer Cell (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- IRIS (submittedVersion)
- SERVAL (Université de Lausanne) (submittedVersion)
- Funders
- AstraZeneca
- Ludwig Institute for Cancer Research
- Genentech
- Sidney Kimmel Foundation
- GlaxoSmithKline
- Neos Therapeutics
- Merck
- Boehringer Ingelheim
- Bristol-Myers Squibb
- Takeda Pharmaceutical Company
- Gilead Sciences (20100111973)
- Astellas Pharma
- Celgene
- AbbVie
- Amgen
- University of Pennsylvania Health System
- Novartis
- Daiichi-Sankyo
- Roche
- Eisai
- Topics
- Health Sciences › Medicine › Oncology › Chemokine receptors and signaling
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Keywords
- RANTES, CXCL9, T cell infiltration, tumor-infiltrating lymphocytes, interferon-gamma, myeloid cells, CXCR3 ligands, DNA methylation, epigenetic silencing, immune checkpoint blockade, tumor surveillance, solid tumors
- MeSH terms
- Antineoplastic Agents, Immunological, Animals, Chemotaxis, Leukocyte, Dendritic Cells, Female, Humans, Immunotherapy, Interferon-gamma, Lymphocyte Activation, Macrophages, Mice, Inbred C57BL, Ovarian Neoplasms, Signal Transduction, Gene Expression Regulation, Neoplastic, Cytokines, Lymphocytes, Tumor-Infiltrating, CD8-Positive T-Lymphocytes, Coculture Techniques, Chemokine CCL5, DNA Methylation, Paracrine Communication, Epigenesis, Genetic, Cell Line, Tumor, Receptors, CXCR3, Chemokine CXCL9
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