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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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“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
“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]
In 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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MethodCutaneous Tumors Cease CXCL9/Mig Production as a Result of IFN-γ–Mediated Immunoediting
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“High expression of CCL3 inmelanomaswas associated with improved recruitment of CD8 effector T cells.(32) Recently, melanoma WNT/β-catenin signaling was shown to prevent anti-tumor immunity and CCL3 expression was repressed by high β-catenin expression.”
BackgroundApplication of CAR T cells for the treatment of solid tumors
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BackgroundDistinct genomic features across cytolytic subgroups in skin melanoma
Roufas, C., Georgakopoulos‐Soares, I., & Zaravinos, A. (2021) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-021-02918-3 · Cited by 17
Immune mechanisms in cancer patients that lead to poor outcomes of SARS-CoV-2 infection
LATIF, M. B., Shukla, S., Estrada, P. M. D. R., Ribeiro, S. P., Sékaly, R., & Sharma, A. (2021) · Translational research · doi:10.1016/j.trsl.2021.12.001 · Cited by 18
Shi, T., & Gao, G. (2022) · Bioscience Reports · doi:10.1042/bsr20212523 · Cited by 18
“271 Besides revealing macrophages, some researchers have found that CXCL10 activates its receptor 272 CXCR3 to induce the infiltration of CD8+ T cells in colorectal cancer[39], breast cancer[40], 273 melanoma[41].”
BackgroundZiman, B., Yang, Q., Zheng, Y., Sheth, M., Nam, C., Zhao, H., Zhang, L., Hu, B., Bhowmick, N. A., Sinha, U. K., et al. (2024) · Cell Death and Disease · doi:10.1038/s41419-024-06488-x · Cited by 17
“To further validate the regulation of FOXM1 on the expression of these immune factors, we selected three chemokines for protein level analysis: CCL2, CXCL9, and CXCL10, given their established roles in directly recruiting T cells (27, 28, 30, 31).”
Current Trends of Immunotherapy in the Treatment of Cutaneous Melanoma: A Review
Naik, P. P. (2021) · Dermatology and Therapy · doi:10.1007/s13555-021-00583-z · Cited by 17
Dysregulation of NK and CD8+T Cells by the Microbiota Promotes the Progression of Lung Cancer
Hu, S., Zha, Y., Yang, W., Cui, K., & Cheng, M. (2022) · Journal of Immunology Research · doi:10.1155/2022/7057089 · Cited by 17
Thomas, J. A., Moly, A. G. G., Xavier, H., Suboj, P., Ladha, A., Gupta, G., Singh, S. K., Palit, P., & Babykutty, S. (2023) · Frontiers in Oncology · doi:10.3389/fonc.2023.1063051 · Cited by 18
“The expression of the pro-inflammatory chemokines CCL5 and CCL2 increased in HIF–1-deficient tumors, which in turn increased the infiltration of cytotoxic lymphocytes into the tumor (50).”
BackgroundPundkar, C. Y., Antony, F., Kang, X., Mishra, A., Babu, R. J., Chen, P., Li, F., & Suryawanshi, A. S. (2023) · Heliyon · doi:10.1016/j.heliyon.2023.e16688 · Cited by 18
“Past studies have shown a positive correlation between increased expression of CCL4 and other chemokine signatures in melanoma metastases with increased infiltration of immune cells (mature DCs, B, and T cells) and favorable patient prognosis [12,105].”
BackgroundCytokine Modification of Adoptive Chimeric Antigen Receptor Immunotherapy for Glioblastoma
Pawlowski, K. D., Duffy, J., Gottschalk, S., & Balyasnikova, I. (2023) · Cancers · doi:10.3390/cancers15245852 · Cited by 16
Jin, P., Civini, S., Zhao, Y., Giorgi, V. D., Ren, J., Sabatino, M., Jin, J., Wang, H., Bedognetti, D., Marincola, F. M., et al. (2014) · British Journal of Cancer · doi:10.1038/bjc.2014.235 · Cited by 17
“It is reasonable to conclude that cancer cells, immune cells, and stromal cells collaborate to develop this favourable inflammatory phenotype (Harlin et al, 2009), but the degree of contribution of each is unclear.”
BackgroundChurch, S., Jensen, S. M., Twitty, C., Bahjat, K. S., Hu, H., Urba, W. J., & Fox, B. A. (2011) · The Cancer Journal · doi:10.1097/ppo.0b013e3182346320 · Cited by 17
A novel non-Hodgkin lymphoma murine model closer to the standard clinical scenario
Bascuas, T., Moreno, M., Mónaco, A., Reyes, L., Paolino, A., Oliver, P., Kramer, M. G., Engler, H., Pacheco, J. P., Grille, S., et al. (2016) · Journal of Translational Medicine · doi:10.1186/s12967-016-1073-8 · Cited by 17
“In melanoma, it has been demonstrated that up regulation of expression of several chemokine genes such as Ccl2, Ccl3, Ccl4, Ccl5, Cxcl9, and Cxcl10 in the tumor microenvironment correlates with the recruitment of activated effector T cells to the tumor increasing antitumor immunity [35].”
BackgroundBroad and Conserved Immune Regulation by Genetically Heterogeneous Melanoma Cells
Neubert, N. J., Tillé, L., Barras, D., Soneson, C., Baumgaertner, P., Rimoldi, D., Gfeller, D., Delorenzi, M., Marraco, S. A. F., & Speiser, D. E. (2017) · Cancer Research · doi:10.1158/0008-5472.can-16-2680 · Cited by 17
“Analysis of whole tumor tissue has previously revealed a 6chemokine signature in biopsies from melanoma metastases that is preferentially expressed in tumors with CTL infiltration (41).”
BackgroundLiu, H., Zhang, Y., Liu, Z., Wang, P., Mo, X., Fu, W., Liu, W., Cheng, Y., & Han, W. (2017) · OncoImmunology · doi:10.1080/2162402x.2017.1292195 · Cited by 17
“expression of chemokines within tumors is associated with increased T-cell infiltration and antitumor response, which is consistent with the previous studies.(30,31) Our data showed”
ResultMooradian, M. J., & Sullivan, R. J. (2017) · Future Oncology · doi:10.2217/fon-2017-0117 · Cited by 18
Tlr7 Agonist in Combination With Salmonella as an Effective Antimelanoma Immunotherapy
Vola, M., Mónaco, A., Bascuas, T., Rimsky, G., Agorio, C., Chabalgoity, J. A., & Moreno, M. (2018) · Immunotherapy · doi:10.2217/imt-2017-0188 · Cited by 17
Cesati, M., Scatozza, F., D’Arcangelo, D., Cappellini, G. A., Rossi, S., Tabolacci, C., Nudo, M., Palese, E., Lembo, L., Lella, G. D., et al. (2020) · Cancers · doi:10.3390/cancers12123680 · Cited by 17
“An additional study reports a significant expression change of six chemokines (namely, CCL2, CCL3, CCL4, CCL5, CXCL9, and CXCL10) related to the lymphocyte infiltration in the melanoma tissue [6].”
BackgroundCyclophosphamide treatment regulates the balance of functional/exhausted tumor-specific CD8+T cells
Hanoteau, A., Henin, C., Švec, D., Donnet, C. B., Denanglaire, S., Colau, D., Romero, P. J., Léo, O., den Eynde, B. J. V., & Moser, M. (2017) · OncoImmunology · doi:10.1080/2162402x.2017.1318234 · Cited by 19
Logan, P. T., Burnier, J. V., & Burnier, M. N. (2016) · ecancermedicalscience · doi:10.3332/ecancer.2013.336 · Cited by 17
McMiller, T. L., Besharati, S., Yarchoan, M., Zhu, Q., Ünsal-Kaçmaz, K., Xu, K., Lee, J., Bhaijee, F., Engle, L. L., Taube, J. M., et al. (2024) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2024-010201 · Cited by 16
The Promise of Targeting Hypoxia to Improve Cancer Immunotherapy: Mirage or Reality?
Janji, B., & Chouaı̈b, S. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.880810 · Cited by 18
Masamoto, Y., Chiba, A., Mizuno, H., Hino, T., Hayashida, H., Sato, T., Bando, M., Shirahige, K., & Kurokawa, M. (2022) · Blood Advances · doi:10.1182/bloodadvances.2022008018 · Cited by 17
Withers, S. S., Moeller, C. E., Quick, C. N., Liu, C., Baham, S. M., Looper, J., Subramanian, R., & Kousoulas, K. G. (2023) · PLoS ONE · doi:10.1371/journal.pone.0284645 · Cited by 22
Geng, P., Chi, Y., Yuan, Y., Yang, M., Zhao, X., Liu, Z., Liu, G., Liu, Y., Zhu, L. W., & Wang, S. (2023) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2023.1158539 · Cited by 15
“As the surfaces of CAR-T cells lack receptors matching the chemokines secreted by solid tumors, CAR-T cells cannot accurately navigate to target tumor sites (Harlin et al., 2009).”
BackgroundLewicky, J. D., Martel, A. L., Gupta, M. R., Roy, R., Rodriguez, G. M., Vanderhyden, B. C., & Le, H. (2023) · Cancers · doi:10.3390/cancers15164127 · Cited by 16
“STING signaling also generates a chemokine gradient, including CXCL10, CCL5, and CXCL9, that can guide the recruitment and activation of T cells [52,64,65] and NK cells [66] within the tumor.”
BackgroundHe, M., Zhang, D., Cao, Y., Chi, C., Zeng, Z., Yang, X., Yang, G., Sharma, K., Hu, K., & Enikeev, M. E. (2023) · Heliyon · doi:10.1016/j.heliyon.2023.e19147 · Cited by 16
“However, cancer cells rarely secrete ligands for CXCR3, thus resulting in the inability of CXCR3-expressing CD8-CAR-Ts to match with cancer cells [96] because cancer cells release chemokines, such as CXCLl5, T cells lack receptors for the relevant chemokines on their surface and therefore fail to recognize tumors [97].”
BackgroundEnhancing T-cell recruitment in renal cell carcinoma with cytokine-armed adenoviruses
Feodoroff, M., Hamdan, F., Antignani, G., Feola, S., Fusciello, M., Russo, S., Chiaro, J., Välimäki, K. E., Pellinen, T. S., Branca, R. M., et al. (2024) · OncoImmunology · doi:10.1080/2162402x.2024.2407532 · Cited by 17
Intestinal Bacteroides drives glioma progression by regulating CD8+ T cell tumor infiltration
Chatterjee, J., Qi, X., Mu, R., Li, X., Eligator, T., Ouyang, M., Bozeman, S. L., Rodgers, R., Aggarwal, S., Campbell, D. E., et al. (2025) · Neuro-Oncology · doi:10.1093/neuonc/noaf024 · Cited by 16
Schuhmacher, B., Rengstl, B., Döring, C., Bein, J., Newrzela, S., Brunnberg, U., Kvasnicka, H. M., Vornanen, M., Küppers, R., Hansmann, M., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.12363 · Cited by 16
“The observation that LP-DLBCL show a high content of CD8-positive T cells in most cases and expression of PDL1 in the tumor cells is similar to the situation observed in other tumors like melanoma, which can basically be divided into tumors with and without recruitment of CD8-positive T cells [44].”
ResultLiu, J., Xu, M., & Yuan, Z. (2020) · BIO Integration · doi:10.15212/bioi-2020-0002 · Cited by 16
Ji, X., Jiang, W., Wang, J., Zhou, B., Ding, W., Liu, S., Huang, H., Chen, G., & Sun, X. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1106644 · Cited by 18
“There is clinical evidence that IFN-I signaling is activated in spontaneously retreating tumors (67) and in metastases highly infiltrated by T cells (68, 69).”
BackgroundSeliger, B. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02043 · Cited by 17
“Members of the CCL and CXCL chemokine families have been associated with T cell recruitment to melanoma metastases (124, 125).”
BackgroundNguyen, M. K., Jelinek, M., Singh, A., Isett, B. R., Myers, E. S., Mullett, S. J., Eisele, Y. S., Beumer, J. H., Parise, R. A., Urban, J. A., et al. (2025) · The Oncologist · doi:10.1093/oncolo/oyaf362 · Cited by 18
Tumor-infiltrating lymphocytes are associated with β-catenin overexpression in breast cancer
Ma, X., Zhao, X., Yan, W., Yang, J. J., Zhao, X., Zhang, H., Hui, Y., & Zhang, S. (2017) · Cancer Biomarkers · doi:10.3233/cbm-170708 · Cited by 15
D’Alise, A. M., Leoni, G., Lucia, M. D., Langone, F., Nocchi, L., Tucci, F. G., Micarelli, E., Cotugno, G., Troise, F., Garzia, I., et al. (2021) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2021-003480 · Cited by 15
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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