Cited by 723Cancer Immunotherapy and BiomarkersChemokine receptors and signalingT-cell and B-cell Immunology

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Intratumoral Activity of the CXCR3 Chemokine System Is Required for the Efficacy of Anti-PD-1 Therapy

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Chow, Melvyn T., Ozga, Aleksandra J., Servis, Rachel L., Frederick, Dennie T., Lo, Jennifer A., Fisher, David E., Freeman, Gordon J., Boland, Genevieve M., Luster, Andrew D.·2019·Immunity

DOI 10.1016/j.immuni.2019.04.010PMC PMC6527362

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Abstract

Despite compelling rates of durable clinical responses to programmed cell death-1 (PD-1) blockade, advances are needed to extend these benefits to resistant tumors. We found that tumor-bearing mice deficient in the chemokine receptor CXCR3 responded poorly to anti-PD-1 treatment. CXCR3 and its ligand CXCL9 were critical for a productive CD8+ T cell response in tumor-bearing mice treated with anti-PD-1 but were not required for the infiltration of CD8+ T cells into tumors. The anti-PD-1-induced anti-tumor response was facilitated by CXCL9 production from intratumoral CD103+ dendritic cells, suggesting that CXCR3 facilitates dendritic cell-T cell interactions within the tumor microenvironment. CXCR3 ligands in murine tumors and in plasma of melanoma patients were an indicator of clinical response to anti-PD-1, and their induction in non-responsive murine tumors promoted responsiveness to anti-PD-1. Our data suggest that the CXCR3 chemokine system is a biomarker for sensitivity to PD-1 blockade and that augmenting the intratumoral function of this chemokine system could improve clinical outcomes.

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“45”
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“We also observed higher mRNA expression levels of the CXCR3 ligand genes CXCL9 and CXCL10 in TLS-positive as compared to TLS-nega-tive tumors, suggesting the recruitment of CD8 + T cells into tumor mass [9].”
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A phase I open label dose‐escalation study to evaluate the tolerability, safety and immunological efficacy of sub‐urothelial durvalumab injection in adults with muscle‐invasive or high‐risk non‐muscle‐invasive bladder cancer (SUBDUE‐1, SUB‐urothelial DUrvalumab injection‐1 study): clinical trial protocol
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IL-2/GM-CSF enhances CXCR3 expression in CAR-T cells via the PI3K/AKT and ERK1/2 pathways
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Sex Differences in the Systemic and Local Immune Response of Pancreatic Cancer Patients
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CRISPR-Cas9 screening identifies an IRF1-SOCS1-mediated negative feedback loop that limits CXCL9 expression and antitumor immunity
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Case report of fatal immune-mediated myocarditis following treatment with davoceticept (ALPN-202), a PD-L1-dependent CD28 costimulator and dual PD-L1/CTLA-4 checkpoint inhibitor, in combination with pembrolizumab
Cavalcante, L. L., Chandana, S. R., Lakhani, N. J., Enstrom, A. M., LeBlanc, H. N., Schmalz, J., Lengyel, K., Schneider, F., Thomas, H., Chisamore, M. J., et al. (2024) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2024-009475 · Cited by 15
“13 14–16 Interestingly, neither patient displayed increased interleukin (IL)- 6 or IL-8, which are cytokines routinely elevated in cytokine release syndrome.”
Synthesis and characterization of soquelitinib a selective ITK inhibitor that modulates tumor immunity
Hsu, L., Rosenbaum, J. T., Verner, E. J., Jones, W. B., Hill, C. M., Janc, J. W., Buggy, J. J., Pawar, R. D., Ghosh, P., Li, D., et al. (2024) · npj Drug Discovery. · doi:10.1038/s44386-024-00002-1 · Cited by 12
T-bet+CD8+ T cells govern anti-PD-1 responses in microsatellite-stable gastric cancers
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IRF1 transcriptionally up-regulates CXCL10 which increases CD8+ T cells infiltration in colorectal cancer
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Chemokines that govern T cell activity in tumors
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An IFNγ/STAT1/JMJD3 Axis Induces ZEB1 Expression and Promotes Aggressiveness in Lung Adenocarcinoma
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“Mol Cancer Res; 19(7) July 2021 MOLECULAR CANCER RESEARCH 1236”
BackgroundInfluential
Cxcr3 constrains pancreatic cancer dissemination through instructing T cell fate
Burrack, A. L., Spartz, E. J., Rollins, M. R., Miller, E. A., Firulyova, M. M., Cruz-Hinojoza, E., Goldberg, M. F., Wang, I., Nanda, H. A., Shen, S., et al. (2022) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-022-03338-7 · Cited by 13
“Cxcr3 promotes T cell migration [11, 12] and PD-1 blockade efficacy [13, 14] in subcutaneous implantable tumor animal models.”
Relationship between chemokine/chemokine receptor and glioma prognosis and outcomes: Systematic review and meta-analysis
Yang, S., Luo, M., Yang, S., Yuan, M., Hu, Z., Xia, J., & Wang, N. (2024) · International Immunopharmacology · doi:10.1016/j.intimp.2024.112047 · Cited by 13
Harnessing the capacity of phytochemicals to enhance immune checkpoint inhibitor therapy of cancers: A focus on brain malignancies
Afshari, A. R., Sanati, M., Ahmadi, S. S., Kesharwani, P., & Sahebkar, A. (2024) · Cancer Letters · doi:10.1016/j.canlet.2024.216955 · Cited by 14
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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“…traf ﬁ cking CD8 +T cells via their CXCR3 receptor 24,28,31 ; CX3CL1 expressed within the TME recruiting CD8 +T cells via their CX3CR1 receptor 29 ; CXCL12 expressed in tumors are involved in homing effector CD8 + T cells via their CXCR4 receptor 28,32 ; CXCL16 ligand expressed by cancer…”
Background
The UBA1–STUB1 Axis Mediates Cancer Immune Escape and Resistance to Checkpoint Blockade
Bao, Y., Cruz, G., Zhang, Y., Qiao, Y., Mannan, R., Hu, J., Yang, F., Gondal, M. N., Shahine, M., Kang, S., et al. (2024) · Cancer Discovery · doi:10.1158/2159-8290.cd-24-0435 · Cited by 16
C-X-C Motif Chemokine Ligand 9 Correlates with Favorable Prognosis in Triple-Negative Breast Cancer by Promoting Immune Cell Infiltration
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Motility Matters: How CD8+ T-Cell Trafficking Influences Effector and Memory Cell DifferentiationPreprint
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Immune Responses in Checkpoint Myocarditis Across Heart, Blood, and TumorPreprint
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Self-citation
Dendritic cells: the central partner for cancer immunity
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IL9 Polarizes Macrophages to M1 and Induces the Infiltration of Antitumor Immune Cells via MIP-1 and CXCR3 Chemokines
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“Recently, intratumoral CD103+ DCs have been robustly reported for their critical roles in trafficking tumor antigen to lymph nodes for both direct CD8+ T-cell stimulation and antigen transfer to resident myeloid cells (39, 40).”
Background
A Novel TrxR1 Inhibitor Regulates NK and CD8+ T Cell Infiltration and Cytotoxicity, Enhancing the Efficacy of Anti–PD-1 Immunotherapy against Hepatocarcinoma
Su, X., Yin, H., Bai, M., Liu, J., Liu, R., Zeng, H., & Wen, J. (2023) · The Journal of Immunology · doi:10.4049/jimmunol.2200389 · Cited by 12
Gene-activating nanomedicine for the tumor-oriented infiltration of T cells to enhance immunotherapy against solid tumors
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The coenzyme A precursor pantethine enhances antitumor immunity in sarcoma
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Transcriptional repression by HDAC3 mediates T cell exclusion from Kras mutant lung tumors
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Advancements in the application of ablative therapy and its combination with immunotherapy in anti-cancer therapy
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Solid Tumor Microenvironment Can Harbor and Support Functional Properties of Memory T Cells
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“A recent study showed that CXCR3 was critical for responsiveness to checkpoint blockade immunotherapy by increasing T cell proximity to intratumoral CD103 DCs in the TME (45).”
Background
CXCR3 isoform A promotes head and neck cancer progression by enhancing stem‐like property and chemoresistance
Sun, W., Peng, T., Tang, S., Lin, J., Wang, C., Fang, H., & Sun, K. (2022) · Journal of Oral Pathology and Medicine · doi:10.1111/jop.13346 · Cited by 12
Stratification of PD-1 blockade response in melanoma using pre- and post-treatment immunophenotyping of peripheral blood
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“ICOS expression on CD8 T cells responding to PD-1 blockade has previously been shown [13], while work by Chow et al . demonstrated that CXCR3 expression is important for α PD-1 efficacy in a mouse tumour model [30].”
Background
HDAC inhibitor HPTA initiates anti-tumor response by CXCL9/10-recruited CXCR3+CD4+T cells against PAHs carcinogenicity
Chen, C., LIM, D. J., Cai, Z., Zhang, F., Liu, G., Dong, C., & Feng, Z. (2023) · Food and Chemical Toxicology · doi:10.1016/j.fct.2023.113783 · Cited by 11
Nuanced role for dendritic cell intrinsic IRE1 RNase in the regulation of antitumor adaptive immunity
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Hepatocellular carcinoma-specific epigenetic checkpoints bidirectionally regulate the antitumor immunity of CD4 + T cells
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Integration of Metabolomics and Transcriptomics to Reveal the Antitumor Mechanism of Dendrobium officinale Polysaccharide-Based Nanocarriers in Enhancing Photodynamic Immunotherapy in Colorectal Cancer
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“Since the CXCR3 chemokine system was reported to be indispensable for the anti–PD-1– mediated response of the CD8 + T cell population residing within melanoma tumors (19), we analyzed the expression of CXCR3 on CD8 + PD-1 + T cells in the SLN tissue by flow cytometry.”
Reciprocal Modulation of Tumour and Immune Cell Motility: Uncovering Dynamic Interplays and Therapeutic Approaches
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Activation of the chemokine receptor 3 pathway leads to a better response to immune checkpoint inhibitors in patients with metastatic urothelial carcinoma
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“However, only a few preclinical experiments have explored the relationship between CXCR3 signaling pathway and cancer immunotherapy [35], and due to the complexity of the immune system, immune responses may vary in different individuals and different types of tumors.”
Background
A risk score combining co-expression modules related to myeloid cells and alternative splicing associates with response to PD-1/PD-L1 blockade in non-small cell lung cancer
Han, Y., Liu, S. M., Jin, R., Meng, W., Wu, Y.-L. L. C., & Li, H. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1178193 · Cited by 11
The level of macrophage migration inhibitory factor is negatively correlated with the efficacy of PD-1 blockade immunotherapy combined with chemotherapy as a neoadjuvant therapy for esophageal squamous cell carcinoma
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Authors: Chow, M. T., Ozga, A. J., Servis, R. L., Frederick, D. T., Lo, J. A., Fisher, D. E., Freeman, G. J., Boland, G. M., & Luster, A. D.
Affiliations: Harvard University (US)
Corresponding author: Luster, Andrew D.
ORCID: Ozga, Aleksandra J.
Frederick, Dennie T.
Lo, Jennifer A.
Fisher, David E.
Freeman, Gordon J.
Boland, Genevieve M.
Luster, Andrew D.
Venue: Immunity
Publisher: Elsevier BV
Published: 2019-06
Volume: 50
Issue: 6
Pages: 1498-1512.e5
ISSN: 1074-7613 (ISSN-L)
DOI: 10.1016/j.immuni.2019.04.010
PMC: PMC6527362
OpenAlex: W2945224722
Cited by: 716
References: 57
Citations by year: 2026: 83 · 2025: 98 · 2024: 120 · 2023: 128 · 2022: 96 · 2021: 90 · 2020: 81 · 2019: 19
FWCI: 30.30
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 384 d)
Locations: Immunity (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (AR043369)
Dr. Miriam and Sheldon G. Adelson Medical Research Foundation
National Institutes of Health (AR043369, CA204028, AI112521, CA222871, CA163222)
Melanoma Research Alliance
Cancer Research Institute
Topics: Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
Health Sciences › Medicine › Oncology › Chemokine receptors and signaling
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Keywords: CXCR3, CXCL9, anti-PD-1 therapy, chemokine system, CD8+ T cells, CD103+ dendritic cells, dendritic cell-T cell interaction, tumor microenvironment, melanoma, predictive biomarkers, immunotherapy resistance
MeSH terms: Antineoplastic Agents, Immunological, Animals, Disease Models, Animal, Humans, Lymphocyte Activation, Neoplasms, Biomarkers, T-Lymphocyte Subsets, Mice, Knockout, CD8-Positive T-Lymphocytes, Xenograft Model Antitumor Assays, Epigenesis, Genetic, Mice, Receptors, CXCR3, Immunomodulation, Molecular Targeted Therapy, Tumor Microenvironment, Programmed Cell Death 1 Receptor

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Intratumoral Activity of the CXCR3 Chemokine System Is Required for the Efficacy of Anti-PD-1 Therapy

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