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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Irradiation Mediates IFNα and CXCL9 Expression in Non-Small Cell Lung Cancer to Stimulate CD8+ T Cells Activity and Migration toward Tumors
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A hepatic network of dendritic cells mediates CD4 T cell help outside lymphoid organs
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Chemokine biology on immune checkpoint–targeted therapies
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Interleukin-34 Limits the Therapeutic Effects of Immune Checkpoint Blockade
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CD8+ T-cell Responses Are Boosted by Dual PD-1/VEGFR2 Blockade after EGFR Inhibition in Egfr -Mutant Lung Cancer
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Single-cell chemokine receptor profiles delineate the immune contexture of tertiary lymphoid structures in head and neck squamous cell carcinoma
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Trackable Intratumor Microdosing and Spatial Profiling Provide Early Insights into Activity of Investigational Agents in the Intact Tumor Microenvironment
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“…locations of drug exposure within the same tumor samples where we observed M1 polarization, we also observed recruitment of CXCR3-expressing cells, including cytotoxic CD8 T and NK cells to regions of SUMOylation inhibition, characteristic of a shift in the TME from “ cold-to-hot ” (46, 47).”
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Oncolytic herpes simplex virus propagates tertiary lymphoid structure formation via CXCL10 / CXCR3 to boost antitumor immunity
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“44,45 Our results suggested that CXCR3 expressed on CD8 + T cells was upregulated in the oHSV therapy group.”
PD-1 and CTLA-4 serve as major gatekeepers for effector and cytotoxic T-cell potentiation by limiting a CXCL9/10-CXCR3-IFNγ positive feedback loop
Abdala-Saleh, N., Lugassy, J., Shivakumar-Kalvhati, A., Turky, A., Ras, S. A., Razon, H., Berger, N., Bar-On, D., Bar‐On, Y., Taura, T., et al. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1452212 · Cited by 25
Dendritic cells instruct T cell anti-tumor immunity and immunotherapy response
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PD-L1 Expression in High-Risk Early-Stage Colorectal Cancer—Its Clinical and Biological Significance in Immune Microenvironment
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Background
Development of a prognostic gene signature based on an immunogenomic infiltration analysis of osteosarcoma
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Phenotypic and spatial heterogeneity of CD8+ tumour infiltrating lymphocytes
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“Cells with both antigen-presenting and immunomodulatory capabilities, especially DCs, are almost invariably implicated in the organisation of these CD8 + T-accommodating alcoves [174, 190, 191, 257–259].”
Background
AMD3100/Plerixafor overcomes immune inhibition by the CXCL12–KRT19 coating on pancreatic and colorectal cancer cells
Fearon, D. T., & Janowitz, T. (2021) · British Journal of Cancer · doi:10.1038/s41416-021-01315-y · Cited by 28
Synthesis and pharmacological evaluation of novel resorcinol biphenyl ether analogs as small molecule inhibitors of PD-1/PD-L1 with benign toxicity profiles for cancer treatment
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Single-cell transcriptomics reveals the effect of PD-L1/TGF-β blockade on the tumor microenvironment
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Dendritic Cell-Based Immunotherapy in Hot and Cold Tumors
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CXCL9 correlates with antitumor immunity and is predictive of a favorable prognosis in uterine corpus endometrial carcinoma
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“revealed that CXCL9 (derived from CD103 dendritic cell) and CD8 T cells (CXCR3 are essential for the efficiency of anti-PD-1 therapy in melanoma, colon adenocarcinoma, and breast adenocarcinoma cell lines (21).”
Background
In situ Vaccination by Direct Dendritic Cell Inoculation: The Coming of Age of an Old Idea?
Castiello, L., Aricò, E., D'Agostino, G., Santodonato, L., & Belardelli, F. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02303 · Cited by 23
“Further, recent literature has unraveled how intratumoral cDC1 “license” CD8 response during checkpoint blockade by secreting IL-12 and CXCL9, potentiating T cell activation (97, 98).”
Background
Structure basis for the modulation of CXC chemokine receptor 3 by antagonist AMG487
Jiao, H., Pang, B., Chiang, Y., Chen, Q., Pan, Q., Ren, R., & Hu, H. (2023) · Cell Discovery · doi:10.1038/s41421-023-00617-0 · Cited by 23
Age-associated changes in the immune system may influence the response to anti-PD1 therapy in metastatic melanoma patients
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T cell infiltration on local CpG-B delivery in early-stage melanoma is predominantly related to CLEC9A+CD141+ cDC1 and CD14+ antigen-presenting cell recruitment
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Both T cell priming in lymph node and CXCR3-dependent migration are the key events for predicting the response of atezolizumab
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T cell–Mediated Development of Stromal Fibroblasts with an Immune-Enhancing Chemokine Profile
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Thirty-five years since the discovery of chemotactic cytokines, interleukin-8 and MCAF: A historical overview
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Combinatorial immunotherapy induces tumor-infiltrating CD8+ T cells with distinct functional, migratory, and stem-like properties
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“37 48–51 Furthermore, the intra-tumoral CXCL9/10-CXCR3 chemokine axis has been shown to play an essential role for the antitumor response mediated by ICB.”
Advances in Cell and Immune Therapies for Melanoma
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CXCR6 + T Cells Drive Immune Checkpoint Inhibitor Myocarditis
Munir, A. Z., Gutierrez, A., Krawiec, C. M., Manandhar, P., Shyani, A. C., Ma, P., Gougis, P., Baylis, R. A., Hou, L., Remold‐O’Donnell, E., et al. (2026) · Circulation · doi:10.1161/circulationaha.125.076976 · Cited by 21
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“Moreover, the biomarker also showed a good predictive effect on different histological types of NSCLC and chemotherapy combined with different PD1 drug groups, it provides a new idea for the biomarkers of tumor combination therapy.”
BackgroundInfluential
A Novel P53 Nanomedicine Reduces Immunosuppression and Augments Anti-PD-1 Therapy for Non-Small Cell Lung Cancer in Syngeneic Mouse Models
Kim, S. S., Harford, J. B., Moghe, M., Doherty, C. L., & Chang, E. H. (2022) · Cells · doi:10.3390/cells11213434 · Cited by 23
“It should be noted that CXCR3-dependent T cell infiltration is a prerequisite to the success of PD-1/PD-L1 blockade therapy [17].”
Background
BayesTME: An end-to-end method for multiscale spatial transcriptional profiling of the tissue microenvironment
Zhang, H., Hunter, M. V., Chou, J., Quinn, J. F., Zhou, M., White, R. M., & Tansey, W. (2023) · Cell Systems · doi:10.1016/j.cels.2023.06.003 · Cited by 22
Tocilizumab and immune signatures for targeted management of cytokine release syndrome in immune checkpoint therapy
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Positioning and reversible suppression of CCR7+ dendritic cells in perivascular tumor niches shape cancer immunity
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Identification of Potential Biomarkers for Anti-PD-1 Therapy in Melanoma by Weighted Correlation Network Analysis
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Programmed death (PD)‐1/PD‐ligand 1 blockade mediates antiangiogenic effects by tumor‐derived CXCL10/11 as a potential predictive biomarker
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CD33 Expression on Peripheral Blood Monocytes Predicts Efficacy of Anti-PD-1 Immunotherapy Against Non-Small Cell Lung Cancer
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“To evaluate the interplay between monocytes and T lymphocytes, we added markers for quantifying the frequencies of CD4+ and CD8+ T cells, including the chemokine receptor CXCR3 (30).”
BackgroundInfluential
Amplification of the CXCR3/CXCL9 axis via intratumoral electroporation of plasmid CXCL9 synergizes with plasmid IL-12 therapy to elicit robust anti-tumor immunity
Lee, J. Y., Nguyen, B., Mukhopadhyay, A., Han, M., Zhang, J., Gujar, R., Salazar, J. V., Hermiz, R., Svenson, L., Browning, E., et al. (2022) · Molecular Therapy — Oncolytics · doi:10.1016/j.omto.2022.04.005 · Cited by 20
“Recent studies have demonstrated a critical role for CXCL9 in facilitating anti-PD-1 checkpoint therapeutic responses.(19,20,34) To investigate this potential relationship, a CT26 tumor model was used to determine whether this increased intratumoral chemokine gradient, particularly in the context of IL-12, could enhan…”
BackgroundMethodSelf-citation
Delivery of CXCL9/10/11 plasmid DNAs promotes the tumor-infiltration of T cells and synergizes with PD1 antibody for treating lung cancer
Ma, Y., Liu, Y., Zhi, Y., Wang, H., Yang, M., Niu, J., Zhao, L., & Wang, P. (2022) · Cancer Nanotechnology · doi:10.1186/s12645-022-00116-z · Cited by 20
“In addition, the intra-tumoral activity of CXCR3 is required for anti-PD-1 therapy efficacy (Chow et al. 2019).”
Background
Role of Exosomes in Immunotherapy of Hepatocellular Carcinoma
Tian, B., Han, C., Dong, Z., Tan, S., Wang, D., & Li, T. (2022) · Cancers · doi:10.3390/cancers14164036 · Cited by 20

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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