Cited by 1,121Chemokine receptors and signalingCancer Immunotherapy and BiomarkersT-cell and B-cell Immunology

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Chemokine Expression in Melanoma Metastases Associated with CD8+ T-Cell Recruitment

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Harlin, Helena, Meng, Yuru, Peterson, Amy C., Zha, Yuanyuan, Tretiakova, Maria, Slingluff, Craig, McKee, Mark, Gajewski, Thomas F.·2009·Cancer Research

DOI 10.1158/0008-5472.can-08-2281PMC PMC3886718

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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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Mutations of the BRAF gene in human cancer
Davies, H., Bignell, G. R., Cox, C., Stephens, P., Edkins, S., Clegg, S., Teague, J., Woffendin, H., Garnett, M. J., Bottomley, W., et al. (2002) · Nature · doi:10.1038/nature00766 · Cited by 10,674
Chemokines
Zlotnik, A., & Yoshie, O. (2000) · Immunity · doi:10.1016/s1074-7613(00)80165-x · Cited by 3,923 · cited 3×
“The indicated chemokines are GRO (1), IL-8 (2 ), CTACK (3), CXCL16 (4 ), IP-10 (5), MCP-1 (6), MIG (7), MIP-1a (8), MIP-1h (9), PARC (10), and RANTES (11 ).”
Background
Chemokines enhance immunity by guiding naive CD8+ T cells to sites of CD4+ T cell–dendritic cell interaction
Castellino, F., Huang, A. Y.-C., Altan-Bonnet, G. Y., Stoll, S., Scheinecker, C., & Germain, R. N. (2006) · Nature · doi:10.1038/nature04651 · Cited by 847 · cited 1×
“Recent work has suggested that CXCR4 and CCR5 may cooperatively provide a costimulatory signal for T-cell activation (16) and that CCR5 on CD8 T cells may be important for the generation of a memory phenotype (17).”
Background
Dacarbazine (DTIC) versus vaccination with autologous peptide-pulsed dendritic cells (DC) in first-line treatment of patients with metastatic melanoma: a randomized phase III trial of the DC study group of the DeCOG
Schadendorf, D., Ugurel, S., Schuler‐Thurner, B., Nestle, F. O., Enk, A., Bröcker, E.-B., Grabbe, S., Rittgen, W., Edler, L., Sucker, A., et al. (2006) · Annals of Oncology · doi:10.1093/annonc/mdj138 · Cited by 470 · cited 2×
“Three chemokine proteins that were reproducibly detected at abundant levels in the tumors with T cells were CCL2/MCP-1, CCL4/MIP-1h, and CCL5/RANTES.”
Tumor Progression Can Occur despite the Induction of Very High Levels of Self/Tumor Antigen-Specific CD8+ T Cells in Patients with Melanoma
Rosenberg, S. A., Sherry, R. M., Morton, K. E., Sharfman, W., Yang, J. C., Topalian, S. L., Royal, R. E., Kammula, U. S., Restifo, N. P., Hughes, M. S., et al. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.175.9.6169 · Cited by 460 · cited 2×
“Because it seemed likely that the protein array approach might not be sensitive enough to detect chemokines in low abundance, real-time RT-PCR was done for expression of CXCL9/Mig, CXCL10/IP-10, and CCL3/MIP-1a.”
Immune resistance orchestrated by the tumor microenvironment
Gajewski, T. F., Meng, Y., Blank, C., Brown, I., Kacha, A., Kline, J., & Harlin, H. (2006) · Immunological Reviews · doi:10.1111/j.1600-065x.2006.00442.x · Cited by 437 · cited 4×
“Numerous putative mechanisms by which tumors can evade immune attack despite the presence of antigen-specific CD8 effector T cells have been proposed and supported by preclinical models (7).”
BackgroundInfluential
Recent Advances in Chemokines and Chemokine Receptors
Zlotnik, A., Morales, J., & Hedrick, J. A. (1999) · Critical Reviews in Immunology · doi:10.1615/critrevimmunol.v19.i1.10 · Cited by 410 · cited 1×
“and positively reinforce recruitment of additional specific T-cell subsets (13).”
Background
Cancer vaccines based on the identification of genes encoding cancer regression antigens
Rosenberg, S. A. (1997) · Immunology Today · doi:10.1016/s0167-5699(97)84664-6 · Cited by 386 · cited 4×
“The indicated chemokines are GRO (1), IL-8 (2 ), CTACK (3), CXCL16 (4 ), IP-10 (5), MCP-1 (6), MIG (7), MIP-1a (8), MIP-1h (9), PARC (10), and RANTES (11 ).”
BackgroundInfluential
Cancer regression in patients with metastatic melanoma after the transfer of autologous antitumor lymphocytes
Rosenberg, S. A., & Dudley, M. E. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0405730101 · Cited by 366 · cited 1×
“Our results have implications for the use of autologous tumorinfiltrating lymphocytes (TIL) as an adoptive transfer immunotherapeutic strategy (23).”
Result
Priming of naive T cells inside tumors leads to eradication of established tumors
Yu, P., Lee, Y., Liu, W., Chin, R., Wang, J. H., Wang, Y., Schietinger, A., Philip, M., Schreiber, H. W., & Fu, Y. (2004) · Nature Immunology · doi:10.1038/ni1029 · Cited by 354 · cited 1×
“Transfection of tumor cells to express LIGHT results in potent tumor rejection (26), and introduction of an adenoviral vector encoding LIGHT can improve the control of preestablished tumors and promote rejection of micrometastases (27).”
Background

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“setting of progression when malignant cells were also detected [19].”
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“One of the earliest studies to link chemokine expression in human melanoma to CD8+ T cell infiltration used gene expression arrays to identify CCL2-5 and CXCL9 as preferentially expressed in T cell rich patients’ tumors (6, 29).”
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“This assumption was supported by our data in Figure 4F showing high expression of the chemokine signature involved in the CD8 T cell recruitment (25) in patients displaying high MHC-I signature, CD8 and NK cells compared to those having low MHC-I signature, CD8 and NK cells.”
Result
Adhesion analysis via a tumor vasculature-like microfluidic device identifies CD8+ T cells with enhanced tumor homing to improve cell therapy
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“In particular, the chemokine genes CCL4, CCL5 and CXCL9, which were found to be diminished in HS versus LS cases from TCGA, were previously reported to be part of a gene signature associated with enhanced T cell infiltration in melanoma [43].”
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IL-27 Induces CCL5 Production by T Lymphocytes, Which Contributes to Antitumor Activity
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“High expression of CCL2, CCL22, and CXCL12 normally attracts immunosuppressive cells (Harlin et al., 2009).”
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Endogenous PGE2 induces MCP-1 expression via EP4/p38 MAPK signaling in melanoma
Tang, M., Wang, Y., HAN, S., Guo, S., Xu, N., & Guo, J. (2012) · Oncology Letters · doi:10.3892/ol.2012.1047 · Cited by 14
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“CXCR3 and CXCR6 are expressed at low levels on naïve T cells, but are upregulated upon activation [39, 40].”
Background
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“It most often binds to the homologous receptor CCR5, a receptor shared by HIV entry into CD4 + T cells (29) , but also binds G-protein-coupled, such as CCR1 and CCR3 (34) .”
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A machine learning model reveals expansive downregulation of ligand-receptor interactions that enhance lymphocyte infiltration in melanoma with developed resistance to immune checkpoint blockade
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“Previous studies investigating chemokines associated with lymphocyte rich TMEs in melanoma observed altered expression of CCL2 , CCL3 , CCL4 , CCL21 , CXCL10 , CXCL11 , and CXCL13 , all of which are ligands expressed by the tumor within the RDI network (Source Data) 22,23 .”
BackgroundInfluential
Integrin β1 activation induces an anti-melanoma host response
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“Moreover, macrophages are a major source of CCL2, CCL3, CCL4, CCL5, CXCL9 and CXCL10, which are important chemokines that induce T lymphocyte chemotaxis, and which we find in association with stromal activation in actual melanomas [49,50].”
Background
Switching on the green light for chimeric antigen receptor T‐cell therapy
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“Moreover, chemokine receptors expressed on T cells frequently do not match the tumor chemokine signature, leading to limited trafficking to the tumor site.(43) Therefore, matching chemokine receptor(s) expressed on CAR T cells to the tumor chemokine milieu is also an attractive strategy as it may allow for a higher fr…”
Background
Systems analysis of barrier molecule and ARNT-related gene expression regulation in melanoma
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Transcriptional and immunohistological assessment of immune infiltration in pancreatic cancer
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“Along with infiltrating cells, omic analyses can inform as to the mutational status of the tumor [8] to identify immunotherapeutic targets [35], and identify expression of inflammatory and chemokine markers that may dictate immune cell recruitment [36, 37].”
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“More specifically, the production of CXCL9 and CXCL10, among other proinflammatory cytokines, has been associated with the severity of melanoma and metastasis (Harlin et al., 2009; Lok et al., 2014).”
Background
Targeting β-catenin using XAV939 nanoparticle promotes immunogenic cell death and suppresses conjunctival melanoma progression
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“Thus, it has been shown that the expression of CCL4, CCL5, and CXCL10 in melanoma metastases is associated with the recruitment of CD8 T cells (68).”
Background
Programming CAR T cells to enhance anti-tumor efficacy through remodeling of the immune system
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“Varying methods have been explored to deliver chemokine receptors into CAR T cells because effective trafficking is also interrupted by the mismatch between the chemokine receptors expressed by CAR T cells and the chemokines expressed by tumors [23].”
Method
The Impact of Tumor Cell-Intrinsic Expression of Cyclic GMP-AMP Synthase (cGAS)-Stimulator of Interferon Genes (STING) on the Infiltration of CD8+ T Cells and Clinical Outcomes in Mismatch Repair Proficient/Microsatellite Stable Colorectal Cancer
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BackgroundInfluential
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“Immunotherapeutic approaches have shown to bene ﬁ t patients with preexisting T-cell responses against their tumor, as evidenced by a baseline CD8 þ T-cell in ﬁ ltration within the tumor microenvironment (43, 44).”
Background
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Background
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“We next tested the impact of FIH on the directional migration of macrophages toward chemokine CCL5, which is known to be associated with an altered myeloid or T cell involvement in melanoma (42–44).”
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Background
Transcriptional repression by HDAC3 mediates T cell exclusion from Kras mutant lung tumors
McGuire, C. K., Meehan, A. S., Couser, E., Bull, L., Minor, A. C., Kuhlmann-Hogan, A., Kaech, S. M., Shaw, R. J., & Eichner, L. J. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2317694121 · Cited by 12
Targeting MARCO in combination with anti-CTLA-4 leads to enhanced melanoma regression and immune cell infiltration via macrophage reprogramming
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“36 39 In contrast, one of the increased chemokines, CCL22, is known for its capacity to recruit regulatory T cells.”
T cell immunotherapy for melanoma from bedside to bench to barn and back: how conceptual advances in experimental mouse models can be translated into clinical benefit for patients
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Background
Payload Delivery: Engineering Immune Cells to Disrupt the Tumour Microenvironment
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“Some studies suggest that its production induces immunosuppression (Chang et al., 2012), while others suggest it promotes tumor immunity (Harlin et al., 2009; Liu et al., 2015).”
Background
Correlation of the tumor escape phenotype with loss of PRELP expression in melanoma
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“Indeed, a positive correlation exists between increased numbers of tumor-infiltrating monocytes and CD8 + T cells and the expression of CCL5 in melanoma, but also in other types of cancer, which further helped the recruitment of CD8 + effector T cells [71, 82, 83].”
Background
Therapeutic Response in Patients with Advanced Malignancies Treated with Combined Dendritic Cell–Activated T Cell Based Immunotherapy and Intensity–Modulated Radiotherapy
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“Once effector cells are generated, they may be released into circulation but fail to reach the targeted site due to lack of a tumor-produced chemokine gradient and/or surface expression of complimentary chemokine receptors that together regulate trafficking of effector cells [30].”
Background
STING-mediated DNA sensing in cancer immunotherapy
Zhou, X., & Jiang, Z. (2017) · Science China Life Sciences · doi:10.1007/s11427-016-9066-0 · Cited by 12
Non-hematopoietic Control of Peripheral Tissue T Cell Responses: Implications for Solid Tumors
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Potential of Mycobacterium tuberculosis chorismate mutase (Rv1885c) as a novel TLR4-mediated adjuvant for dendritic cell-based cancer immunotherapy
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Background
Radiotherapy for HPV-related cancers: prediction of therapeutic effects based on the mechanism of tumor immunity and the application of immunoradiotherapy
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Development of Small-Molecule STING Activators for Cancer Immunotherapy
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NLRC3 High Expression Represents a Novel Predictor for Positive Overall Survival Correlated With CCL5 and CXCL9 in HCC Patients
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“Cancer cells can inhibit CCL5 expression because it attracted CD8T cells (33).”
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Cancer Vaccine in Cold Tumors: Clinical Landscape, Challenges, and Opportunities
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STING signalling compensates for low tumour mutation burden to drive anti-tumour immunity
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The CXCL10/CXCR3 axis is essential for sustaining immunological dormancy in triple-negative breast cancer
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Reversing Chemokine/Chemokine Receptor Mismatch to Enhance the Antitumor Efficacy of CAR-T Cells
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Intratumoral IFN-γ or topical TLR7 agonist promotes infiltration of melanoma metastases by T lymphocytes expanded in the blood after cancer vaccine
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“Immune cells and cytokines play essential roles in tumor microenvironment and immune homeostasis (Harlin et al., 2009; Peng et al., 2012), which can be utilized by immunotherapy and contribute to the development of irAEs.”
Background
A PRMT5-ZNF326 axis mediates innate immune activation upon replication stress
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“As further evidence that the modulation of chemokine patterns might be used by tumours to control the trafficking of T cells the induction of specific chemokine ligands in melanoma triggers the recruitment of T cells to the tumour site.(55) Tumour-derived microvesicles have been shown to induce secretion of CXCL8, CCL…”
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“At the same time, chemokines can also recruit CD8+ T cells to inhibit tumour progression (29, 30).”
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Applications of molecular engineering in T‐cell‐based immunotherapies
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“…success of CAR T-cells in treating leukemic and lymphoblastic cancers has yet to be realized in treating solid tumors, in which the immunosuppressive microenvironment, lack of cancer-specific targets, and heterogeneity of the cancer cell population hinder CAR T-cell function(Harlin et al., 2009).”
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Immune Profiling Reveals Molecular Classification and Characteristic in Urothelial Bladder Cancer
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“The antitumor T cell response is crucial for immunotherapy, such as immune checkpoint inhibitors, to function (Harlin et al., 2009; Ji et al., 2012; Liu, 2019).”
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Machine Learning for Future Subtyping of the Tumor Microenvironment of Gastro-Esophageal Adenocarcinomas
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Triggering immunogenic death of cancer cells by nanoparticles overcomes immunotherapy resistance
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Intratumoral administration of mRNA COVID-19 vaccine delays melanoma growth in mice
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“Although these results were obtained in a small series of patients, the results are in line with previous studies indicating a link between ISG expression and presence of TILs in melanomas.(4,23) When comparing receptor expression on TILs and PBMCs, the TILs showed higher expression of CCR5 and PD-1 but tended to expr…”
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Burchett, R., Walsh, S. R., Wan, Y., & Bramson, J. L. (2020) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2020.07.003 · Cited by 9
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IL-12 conditioning of peripheral blood mononuclear cells from breast cancer patients promotes the zoledronate-induced expansion of γδ T cells in vitro and enhances their cytotoxic activity and cytokine production
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STAT4, a potential predictor of prognosis, promotes CD8 T‑cell infiltration in ovarian serous carcinoma by inducing CCL5 secretion
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CDK4/6i enhances the antitumor effect of PD1 antibody by promoting TLS formation in ovarian cancer
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“In addition, melanomas can secrete immunosuppressive cytokines and chemokines, including TGF-b and IL-6,(28) while simultaneously failing to produce immune-attracting factors such as CCL2, CCL3, CCL4, CCL5, CXCL9 and CXCL10, all of which have been shown to be responsible for the recruitment of Teffs and associated eff…”
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Immunodiagnostics and Immunotherapy Possibilities for Prostate Cancer
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“Besides, the chemokine receptors on T cells often fail to match the signature of tumor cells, resulting in less migration to the tumor area (7).”
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Adenosine-Deaminase-Acting-on-RNA-1 Facilitates T-cell Migration toward Human Melanoma Cells
Margolis, N., Moalem, H., Meirson, T., Galore-Haskel, G., Markovits, E., Baruch, E. N., Vizel, B., Yeffet, A., Kanterman-Rifman, J., Debby, A., et al. (2022) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-21-0643 · Cited by 9
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Improved melanoma survival at last! Ipilimumab and a paradigm shift for immunotherapy
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Definition of Key Variables for the Induction of Optimal NY-ESO-1–Specific T Cells in HLA Transgene Mice
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IP-10 enhances the amplification capacity and antitumor activity of CAR-T cells in vitro and could influence positive outcomes in MM patients treated with CAR-T cell therapy
Liu, T., Long, X., Zhang, Y., Jin, J., Chen, L., & Liu, A. (2022) · International Immunopharmacology · doi:10.1016/j.intimp.2022.109253 · Cited by 8
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Advances in nanoplatform-based multimodal combination therapy activating STING pathway for enhanced anti-tumor immunotherapy
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KRAS mRNA Spleen‐Targeting Lipid Nanoparticles Synergize with Irinotecan Silicasomes to Robustly Augment the Cancer Immunity Cycle in Pancreatic Cancer
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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)
ORCID: Peterson, Amy C.
Zha, Yuanyuan
Tretiakova, Maria
Slingluff, Craig
McKee, Mark
Gajewski, Thomas F.
Venue: Cancer Research
Publisher: American Association for Cancer Research (AACR)
Published: 2009-04-01
Volume: 69
Issue: 7
Pages: 3077-3085
ISSN: 0008-5472 (ISSN-L)
1538-7445
DOI: 10.1158/0008-5472.can-08-2281
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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Chemokine Expression in Melanoma Metastases Associated with CD8+ T-Cell Recruitment

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