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Chemokine Expression in Melanoma Metastases Associated with CD8+ T-Cell Recruitment
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Abstract
Despite the frequent detection of circulating tumor antigen-specific T cells, either spontaneously or following active immunization or adoptive transfer, immune-mediated cancer regression occurs only in the minority of patients. One theoretical rate-limiting step is whether effector T cells successfully migrate into metastatic tumor sites. Affymetrix gene expression profiling done on a series of metastatic melanoma biopsies revealed a major segregation of samples based on the presence or absence of T-cell-associated transcripts. The presence of lymphocytes correlated with the expression of defined chemokine genes. A subset of six chemokines (CCL2, CCL3, CCL4, CCL5, CXCL9, and CXCL10) was confirmed by protein array and/or quantitative reverse transcription-PCR to be preferentially expressed in tumors that contained T cells. Corresponding chemokine receptors were found to be up-regulated on human CD8(+) effector T cells, and transwell migration assays confirmed the ability of each of these chemokines to promote migration of CD8(+) effector cells in vitro. Screening by chemokine protein array identified a subset of melanoma cell lines that produced a similar broad array of chemokines. These melanoma cells more effectively recruited human CD8(+) effector T cells when implanted as xenografts in nonobese diabetic/severe combined immunodeficient mice in vivo. Chemokine blockade with specific antibodies inhibited migration of CD8(+) T cells. Our results suggest that lack of critical chemokines in a subset of melanoma metastases may limit the migration of activated T cells, which in turn could limit the effectiveness of antitumor immunity.
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“Tumors from patients showing sustained treatment response predominately demonstrate a T cell-inflamed tumor microenvironment prior to, or early on, treatment.”
From Reimagining IDO Pathway Inhibition in Cancer Immunotherapy via Downstream Focus on the Tryptophan–Kynurenine–Aryl Hydrocarbon Axis (2019) · cites this paper as [6]
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“an effector population shown to be a target of downstream STING signaling involving the IFN-β-CXCL9/10 axis.54–58”
From Functional tumor cell-intrinsic STING, not host STING, drives local and systemic antitumor immunity and therapy efficacy following cryoablation (2023) · cites this paper as [55]
Experimental — accuracy not yet measuredIn the citing paper
“Tumor analysis from patients with metastatic melanoma receiving vaccine and cytokine therapies suggested a paradigm of two broad phenotypes characterized by the presence or absence a T cell-inflamed tumor.”
From Reimagining IDO Pathway Inhibition in Cancer Immunotherapy via Downstream Focus on the Tryptophan–Kynurenine–Aryl Hydrocarbon Axis (2019) · cites this paper as [6]
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Citations
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Background
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“We observed, in different disease models, their presence; studies in humans have identified these signatures to be associated with improved survival of patients with colon, lung and ovarian cancer or melanoma (Benencia et al. 2005; Pages et al. 2005; Dieu-Nosjean et al. 2008; Camus et al. 2009; Galon et al. 2006, 2007…”
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“A previous study has shown that tumors with T cell exclusion have angiogenic factors with high expression level, resulting in promotion of tumor metastasis (Harlin et al., 2009).”
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“Additionally, CXCL9, CXCL10, and CXCL13 are involved in attracting CD8 effector T cells, and a high infiltration of T lymphocytes has been linked to improved survival outcomes (Sato et al., 2005; Harlin et al., 2009; Ukita et al., 2022).”
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“These chemokines were uniquely selected in view of their importance in lymphocyte recruitment (Harlin et al., 2009 ), their role in host re - sponse against cancer, and the contribution of IL-6 and IL-8 as proto-typic senescence-associated secretory phenotype (SASP) components (Kumari & Jat, 2021 ).”
Immune-Mediated Tumor Rejection
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Stromal CD4+ and CD8+ T Cells in Human Breast Carcinomas. Its Correlation with Chemokine MIG/CXCL9
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“38% of participants had a CR with NED for a median of 59 months (2-334).”
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BackgroundImmunotherapy in Head and Neck Squamous Cell Carcinoma (HNSCC)
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“CXCL9 and CXCL11 have been associated with activation of Th1 immunity within TME and a favorable response to chemotherapy and immunotherapy in melanoma (Harlin et al., 2009; Hong et al., 2011).”
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Intratumoral administration of mRNA-1273 vaccine delays melanoma growth in micePreprint
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“35-38 A single intratumoral injection of mRNA-1273 vaccine significantly delays tumor growth.”
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Rare primary anorectal malignant melanoma presenting with painless hematochezia: a case report
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The critical role of homing in TIL therapy success: From biology to clinical application
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“Evidence from melanoma demonstrates that higher CD8 + T-cell infiltration was linked to increased chemokine expression, highlighting the importance of matching chemokine receptors and ligands for T-cell trafficking [44, 45].”
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“However, the migration of T cells is inhibited when a CCL5-specific antagonist is used [31].”
TBC1 domain family member 23 is essential for STING-mediated anti-melanoma effect
Niu, S., Li, G., Wei, P., Hu, X., Qin, J., Yuan, Y., Wang, J., Tu, Y., Zhao, L., Yu, L., et al. (2026) · Molecular Biomedicine · doi:10.1186/s43556-026-00418-3 · Cited by 1
“A critical determinant of therapeutic efficacy, the tumor immune microenvironment orchestrates antitumor immune responses, with cytotoxic CD8 ⁺ T lymphocytes and natural killer (NK) cells serving as the principal effectors in this intricate niche [33, 34].”
Li, W., Sun, J., Tian, H., Tang, X., Gao, L., Liang, S., Zhang, Z., Sun, Y., Ma, J., & Zhao, X. (2026) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2025-014258 · Cited by 1
Kurosaki, T., Suzuki, S., Watanabe, Y., Kenmotsu, H., Itoh, S., Yamaguchi, M., Shiono, A., Suzuki, T., Yokoyama, T., Toi, Y., et al. (2026) · Lung Cancer · doi:10.1016/j.lungcan.2026.109416 · Cited by 1
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“65 – 68 In addition to shaping the immune compartment, MSI and MSS CRCs differ in tumor cell – intrinsic programmes.”
Biomarkers for predicting and monitoring the efficacy of cancer vaccines
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“Gene expression is most often used as a biomarker to determine the immune status of a tumor (126, 137, 138).”
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Cancer Immunotherapy: Overview in Brief
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CAR-T Therapy for Solid Tumors: Development of New Strategies
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Type I Interferons: History and Perspectives as Immunotherapeutic Agents Against Cancer
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The Role of the Immune System and Immunoregulatory Mechanisms Relevant to Melanoma
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“Melanoma patients having T-cell-infl amed tumors showed expression of a chemokine signature for T-cell recruitment (CCL2, CCL3, CCL4, CCL5, CXCL9, and CXCL10) had a more favorable clinical outcome [ 9 , 30 ].”
BackgroundInfluentialHoming Improvement: Boosting T Cell Trafficking for Cancer Immunotherapy
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Activated melanoma vessels: A sticky point for successful immunotherapy
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Involvement of STING signaling pathway in non-alcoholic fatty liver disease
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The Impact of the Extracellular Matrix on Immunotherapy Success
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Macrophage Response to Simulated Solar Radiation in the Development of Human Malignant Melanoma
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Characterization of the Role of CXCL10 and CXCR3 in Breast Cancer
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CRY1 fuels resistance to T cell-based immunotherapy in NANOGhigh cancersPreprint
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“Also, the local chemokine milieu can have profound effects on whether T cells traffic to tumors (Harlin et al., 2009).”
BackgroundThe role of D6 in neutrophil migration, melanoma growth and metastasis
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Neue Therapiestrategien beim malignen Melanom
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Personalized Immunotherapy: A Siren Myth?
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THE ROLE OF HEAT SHOCK PROTEIN RECEPTOR CD91 IN INITIATION OF TUMOR-ASSOCIATED IMMUNITY
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Recombinant protein vaccination for antigen-specific cancer immunotherapy
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“Andere Untersucher stellten 3 Chemokin-Proteine auf hohem Niveau reproduzierbar in den Melanomtumoren fest: CCL2/MCP-1, CCL4/MIP-1β und R/C [26].”
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Melanoma & biomarkers of immunoresponsiveness
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Novel Immunotherapies and Novel Combinations of Immunotherapy
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Metadata
- Authors
- Harlin, H., Meng, Y., Peterson, A. C., Zha, Y., Tretiakova, M., Slingluff, C., McKee, M., & Gajewski, T. F.
- Affiliations
- 1Department of Pathology,
- 2Department of Medicine, Section of Hematology/Oncology, and
- University of Virginia (US)
- University of Chicago (US)
- Venue
- Cancer Research
- Published
- 2009-04-01
- Volume
- 69
- Issue
- 7
- Pages
- 3077-3085
- ISSN
- 0008-5472 (ISSN-L)
- 1538-7445
- PMC
- PMC3886718
- OpenAlex
- W2162222767
- Cited by
- 1,121
- References
- 29
- Citations by year
- 2026: 40 · 2025: 58 · 2024: 89 · 2023: 95 · 2022: 118 · 2021: 121 · 2020: 105 · 2019: 87 · 2018: 69 · 2017: 77 · 2016: 51 · 2015: 42 · 2014: 29 · 2013: 37 · 2012: 28
- FWCI
- 17.00
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Cancer Research (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Burroughs Wellcome Fund
- University of Chicago
- National Cancer Institute (P01CA97296, R01 CA90575, R01CA090575, P01CA097296, P30CA044579)
- Topics
- Health Sciences › Medicine › Oncology › Chemokine receptors and signaling
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Keywords
- melanoma metastasis, chemokines, CD8+ T cell recruitment, T cell migration, MCP-1, CCL3, carbon tetrachloride, RANTES, CXCL9, CXCL10, chemokine receptors, tumor immune microenvironment, chemokine blockade, antitumor immunity, melanoma cell lines, xenografts
- MeSH terms
- Cell Movement, Multigene Family, Humans, Melanoma, Gene Expression, CD8-Positive T-Lymphocytes, Chemokines, Protein Array Analysis, Cell Line, Tumor
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