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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Additional file 7 of 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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Additional file 1 of 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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Additional file 3 of 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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Additional file 1 of Co-enrichment of CD8-positive T cells and macrophages is associated with clinical benefit of tislelizumab in solid tumors
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Additional file 5 of CXCR3 predicts the prognosis of endometrial adenocarcinoma
Dong, H. Y., Sun, M., Li, H., & Yue, Y. (2023) · Figshare · doi:10.6084/m9.figshare.22600238
Additional file 8 of CXCR3 predicts the prognosis of endometrial adenocarcinoma
Dong, H. Y., Sun, M., Li, H., & Yue, Y. (2023) · Figshare · doi:10.6084/m9.figshare.22600247
Additional file 4 of CXCR3 predicts the prognosis of endometrial adenocarcinoma
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Additional file 2 of Expression profile and prognostic value of CXCR family members in head and neck squamous cell carcinoma
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Additional file 5 of 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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Additional file 1 of Single-cell transcriptomics reveals the effect of PD-L1/TGF-β blockade on the tumor microenvironment
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Additional file 7 of CXCR3 predicts the prognosis of endometrial adenocarcinoma
Dong, H. Y., Sun, M., Li, H., & Yue, Y. (2023) · Figshare · doi:10.6084/m9.figshare.22600244
Additional file 6 of CXCR3 predicts the prognosis of endometrial adenocarcinoma
Dong, H. Y., Sun, M., Li, H., & Yue, Y. (2023) · Figshare · doi:10.6084/m9.figshare.22600241
Additional file 4 of Activation of the chemokine receptor 3 pathway leads to a better response to immune checkpoint inhibitors in patients with metastatic urothelial carcinoma
Feng, W., Lin, A., Sun, L., Wei, T., Ying, H., Zhang, J., Luo, P., & Zhu, W. (2022) · Figshare · doi:10.6084/m9.figshare.19766168
Additional file 6 of Activation of the chemokine receptor 3 pathway leads to a better response to immune checkpoint inhibitors in patients with metastatic urothelial carcinoma
Feng, W., Lin, A., Sun, L., Wei, T., Ying, H., Zhang, J., Luo, P., & Zhu, W. (2022) · Figshare · doi:10.6084/m9.figshare.19766177
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Additional file 1 of Expression profile and prognostic value of CXCR family members in head and neck squamous cell carcinoma
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TMEM33 deletion potentiates anti-tumor CD8 + T cell immunityPreprint
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When genetics meets immunology: the assessment of genetic and immunological backgrounds in advanced NSCLC patients treated with immunotherapy – preliminary study
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CXCL10 Expression Predicts Favorable Prognosis and Defines an Interferon-Driven Immune-Active Phenotype in Skin Cutaneous Melanoma
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Significance of Measuring Interferon-γ-Induced Protein-10 Levels in Patients Receiving Systemic Therapies for Unresectable Hepatocellular Carcinoma
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“In recent studies, intra-tumoral CD8 T-cell infiltration was observed with IP-10 upregulation by regorafenib plus PD-1 blockade combination therapy [32, 33].”
APR-246 drives ROS-dependent ferroptosis and apoptosis and enhances anti–PD-1 efficacy in bladder cancer
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Impact of GM-CSF and Two-Site Vaccination on Clinical Outcomes after Multipeptide Vaccination for Melanoma: Long-term Analysis of a Randomized Phase II Trial
Ninmer, E. K., Zhu, H., Sarkar, A., Chianese‐Bullock, K. A., Ross, M. I., Haas, N. B., von Mehren, M., Boisvert, M. E., Kirkwood, J. M., & Slingluff, C. L. (2026) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-25-4606
Etude des mécanismes moléculaires conférant aux cellules dendritiques XCR1+ leurs capacités à activer les lymphocytes cytotoxiques au cours d'une réponse antivirale et antitumorale
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Decoding the cellular interactions regulating CAR T cell antitumor activity in vivo using two-photon intravital imaging
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Etude de l’influence du TGF-β sur les sous-populations de fibroblastes associés au cancer et leur implication pronostique dans les cancers du pancréas
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Identification of Biomarkers Associated With the Combination of Immunotherapy and Anti-Angiogenic Drugs in the Treatment of Mesothelioma : Translational Analyses of the PEMBIB Clinical Trial Combining the Anti-PD1 Monoclonal Antibody Embrolizumab and the Anti-Angiogenic Tyrosine Kinase Inhibitor Nintedanib
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Cardiac tertiary immune niches drive immune activation in immune checkpoint inhibitor myocarditis
Tymm, C. C., Paiola, M., Bukhari, S., Hu, X., WINCHESTER, R. J., & Mor, A. (2026) · Science Advances · doi:10.1126/sciadv.aed8359
Defining the differential contributions of CD4+ and CD8+ T cells to CAR T cell therapy against B cell malignancies
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Ultrasons thérapeutiques pour application en oncologie : optimisation de thérapies thermique et mécanique avec un système confocal pour des traitements combinés, et développement de nanoparticules pour une activation immunitaire
Dahan, M. (2023) · theses.fr (ABES) · doi:10.70675/ba071bbczf50bz4de2za53ez46adb6d11631
Effet des inhibiteurs de la pompe à proton gastrique sur la réponse anti tumorale aux inhibiteurs de point de contrôle immunitaire
Ramel, E. (2024) · theses.fr (ABES) · doi:10.70675/32b76beaz4116z4679z82fbze0b633f58b0e
Influence des neurones sensoriels sur la croissance tumorale et sur la réponse immunitaire anti-tumorale associée
Mardelle, U. (2024) · theses.fr (ABES) · doi:10.70675/1e786d9ez8d0ez41b3z8ac1z367faf59ae53
USP13 stabilizes SOCS1 to reverse αPD-1 resistance in MSI-H colorectal cancer
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Tumor‐Intrinsic ARHGEF3 Enhances Antitumor Immunity by Promoting T‐Cell Infiltration and Limiting Myeloid Cell‐Mediated Immunosuppression
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Growth hormone receptor antagonism improves tumoral chemo-immunotherapy response in a mouse model of lung cancer
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“Similarly, expression of the chemokine receptor CXCR3 has been reported as a predictive biomarker of response to PD-1 blockade in mouse models of colon cancer, whereas such an association has not been demonstrated in NSCLC [19] .”
MORPHEUS-Lung: biomarkers and clinical response to atezolizumab + bevacizumab + stereotactic body radiotherapy in patients with metastatic non-small cell lung cancer
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Glucocorticoids induce a phagocytic C1Q+ macrophage phenotype primed for IFNγ-dependent CXCL9 secretion
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“This ligand of the CXCR3 chemokine system has already been shown to be required for the efficacy of anti-PD-1 therapy in several cancer models 50–53 .”
Immune checkpoint co-expression combined with systemic inflammatory index: A promising approach in prognostic evaluation of lymphoma in Egypt
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Immunotherapy response and resistance in endometrial cancer: Integrating molecular subtype, spatial immune states, and pharmacodynamic biomarkers
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Poorly perfused tumor regions harbor T cells with a glucose-dependent effector phenotype
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“CXCR3 is the receptor of IFN-induced chemokines CXCL9, CXCL10 and CXCL11, and activation of CXCR3 signaling in CD8 TILs has been shown to enhance their antitumor function and anti-PD-1-mediated activity (Peng et al, 2015; Chow et al, 2019; Dangaj et al, 2019).”
High-dimensional immune profiling of peripheral blood identifies immune correlates of anti-PD-1/PD-L1 resistance in oncogenic driver mutation-positive NSCLC
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Circulating cell populations as response predictors and targets to improve immunotherapy in metastatic lung cancer
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CXCL10-driven STAT3 signaling programs pathogenic CD4+ T cell responses and limits antiviral immunity during arthritogenic alphavirus infectionPreprint
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CXCL13-expressing CD4 + T cells coordinate the lymphocytes triad to promote the anti-tumor immunity in NSCLC
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Metabolic inhibition of glutamate-cysteine ligase increases dendritic cell-mediated antitumor immunity in melanoma
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Tailored FcγR blockade enhances immune checkpoint therapy and overcomes resistance
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Integrating biology and mathematics to understand checkpoint immunotherapy
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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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