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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Background
Chemokines enhance immunity by guiding naive CD8+ T cells to sites of CD4+ T cell–dendritic cell interaction
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Background
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BackgroundInfluential
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Result
Priming of naive T cells inside tumors leads to eradication of established tumors
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Background

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Background
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Background
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Background
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Background
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Background
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Background
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The Cancer Cell Dissemination Machinery as an Immunosuppressive Niche: A New Obstacle Towards the Era of Cancer Immunotherapy
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Cutting Edge: Engineering Active IKKβ in T Cells Drives Tumor Rejection
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Background
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Dissecting the Tumor–Immune Landscape in Chimeric Antigen Receptor T-cell Therapy: Key Challenges and Opportunities for a Systems Immunology Approach
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Prognostic Biomarkers and Immunotherapeutic Targets Among CXC Chemokines in Pancreatic Adenocarcinoma
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Background
Leveraging STING, Batf3 Dendritic Cells, CXCR3 Ligands, and Other Components Related to Innate Immunity to Induce a “Hot” Tumor Microenvironment That Is Responsive to Immunotherapy
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Baseline and post-treatment biomarkers of resistance to anti-PD-1 therapy in acral and mucosal melanoma: an observational study
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Bladder cancer intrinsic LRFN2 drives anticancer immunotherapy resistance by attenuating CD8 + T cell infiltration and functional transition
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MHC-class I-restricted CD4 T cells: a nanomolar affinity TCR has improved anti-tumor efficacy in vivo compared to the micromolar wild-type TCR
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Innate and Adaptive Immune Cell Metabolism in Tumor Microenvironment
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“A subset of chemokines (CCL2, CCL3, CCL4, CCL5, CXCL9, and CXCL10) was also preferentially expressed in pre-treatment melanoma metastases infiltrated with CD8+ T cells [12].”
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Cancer immunotherapy for metastasis: past, present and future
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PD-1 Blockade Following Isolated Limb Perfusion with Vaccinia Virus Prevents Local and Distant Relapse of Soft-tissue Sarcoma
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Background
Rapid recovery of postnivolumab vemurafenib-induced Drug Rash with Eosinophilia and Systemic Symptoms (DRESS) syndrome after tocilizumab and infliximab administration
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The heterogeneity of tumor-infiltrating CD8+ T cells in metastatic melanoma distorts their quantification: how to manage heterogeneity?
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Nuclear translocation of plasma membrane protein ADCY7 potentiates T cell-mediated antitumour immunity in HCC
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“34 By integrating the above results, two genes ( ADCY7 and Fc fragment of IgE receptor 1 g, FCER1G ) that were strongly correlated with T cell-mediated immunity (Pearson r>0.5 and p 0.05) were preliminarily selected (figure 1E,F, online supplemental table 6).”
Influential
In Vitro and in Vivo Anticancer Activity of a Synthetic Glycolipid as Toll-like Receptor 4 (TLR4) Activator
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Chemokine profiling in serum from patients with ovarian cancer reveals candidate biomarkers for recurrence and immune infiltration
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“…cell carcinoma clinical trials reported the association of intratumoral CXCL9 and CXCL10 in TILs with clinical benefit from adoptive T cell therapy (69), ipilim-umab (70,71) and pembrolizumab (72), as well as the increase of circulating CXCL9 and CXCL10 during treatment with nivolumab (73,74).”
Vasculogenic mimicry structures in melanoma support the recruitment of monocytes
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“CXCL9 and CXCL10 as well as CXCL11 and CCL5 have been well-known as important chemokines for CD8 + T-cell trafficking [35], and the STING pathway is one of the crucial signaling pathways to regulate the expression of those chemokines [36].”
Background
Going (Reo)Viral: Factors Promoting Successful Reoviral Oncolytic Infection
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“Tumours can furthermore prevent the expression of T cell attractive chemokines such as CCL2, 3, 4, 5, 9 and 10, which may hinder trafficking of T cells to tumour beds [10,139].”
Background
The Barrier Molecules Junction Plakoglobin, Filaggrin, and Dystonin Play Roles in Melanoma Growth and Angiogenesis
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The Interplay between Tumour Microenvironment Components in Malignant Melanoma
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N6-Methyladenosine in Cancer Immunotherapy: An Undervalued Therapeutic Target
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Association of KDR Mutation With Better Clinical Outcomes in Pan-Cancer for Immune Checkpoint InhibitorsPreprint
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Mavorixafor, an Orally Bioavailable CXCR4 Antagonist, Increases Immune Cell Infiltration and Inflammatory Status of Tumor Microenvironment in Patients with Melanoma
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“Elevated expression of these chemokine receptors in solid tumors promotes CD8+ T-cell responses and is associated with positive overall responses in patients with metastatic melanoma (42, 43).”
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Regulation of pancreatic cancer therapy resistance by chemokines
Gautam, S. K., Basu, S., Aithal, A., Dwivedi, N. V., Gulati, M., & Jain, M. (2022) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2022.08.010 · Cited by 26
CEBPB is associated with active tumor immune environment and favorable prognosis of metastatic skin cutaneous melanoma
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“For example, the migration of T cells from the second lymphoid organ to the solid tumor tissue is regulated by some chemokines (10).”
Background
Immune signature of pheochromocytoma and paraganglioma in context of neuroendocrine neoplasms associated with prognosis
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“…T cells, overexpressed in non-metastatic compared to metastatic PCPGs. CCL3/CCL4 have been implicated in the recruitment of NK cells and directing CD8 + T cells in ﬁ ltration into the primary tumor site and hence they are potentially important chemokines for directing anti-tumor immunity [35, 36].”
CX3CR1 deficiency-induced TIL tumor restriction as a novel addition for CAR-T design in solid malignancies
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Tumor Immunophenotyping‐Derived Signature Identifies Prognosis and Neoadjuvant Immunotherapeutic Responsiveness in Gastric Cancer
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Anti-cancer activity of Annexin V in murine melanoma model by suppressing tumor angiogenesis
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Molecular markers in melanoma
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IFN-γ in tissue-immune homeostasis and antitumor immunity
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Targeting the NANOG/HDAC1 axis reverses resistance to PD-1 blockade by reinvigorating the antitumor immunity cycle
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Molecular Characteristics of T Cell-Mediated Tumor Killing in Hepatocellular Carcinoma
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Exercise accelerates recruitment of CD8+ T cell to promotes anti-tumor immunity in lung cancer via epinephrine
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Background
Targeted overexpression of prostacyclin synthase inhibits lung tumor progression by recruiting CD4+ T lymphocytes in tumors that express MHC class II
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“metastatic melanoma.(21) To evaluate whether the increase in tumor-infiltrating CD4C T cells observed in pulmonary PGIS overexpressing mice is mediated by these cytokines, total RNA was extracted from tumor-bearing lungs and expression of CXCL9 and CXCL10 was determined by quantitative RT-PCR (Fig.”
Method
SQSTM1/p62 regulate breast cancer progression and metastasis by inducing cell cycle arrest and regulating immune cell infiltration
Qi, J., He, J., Liu, C.-B., Jin, S.-M., Yang, X., Bai, H., & Ma, Y. (2021) · Genes & Diseases · doi:10.1016/j.gendis.2021.03.008 · Cited by 26
“Expression of CCL2/3/4/5 and CXCL9/10 is associated with the presence of tumor infiltrating lymphocytes (TILs) and Th1 immunity activation in melanoma.(38) In breast cancer, high expression of CXCR4, CCR7 and CXCL12 has a critical role in determining the metastatic phenotype.”
Preliminary Computed Tomography Radiomics Model for Predicting Pretreatment CD8+ T-Cell Infiltration Status for Primary Head and Neck Squamous Cell Carcinoma
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Advances and Hurdles in CAR T Cell Immune Therapy for Solid Tumors
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“Similarly, lung tumors secreting high levels of CCL2 can be efficiently eradicated by CAR T cells targeting mesothelin and concomitantly expressing the CCL2 receptor CCR2b [3,4].”
Background

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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