Oxaliplatin, ATR inhibitor and anti-PD-1 antibody combination therapy controls colon carcinoma growth, induces local and systemic changes in the immune compartment, and protects against tumor rechallenge in mice
BackgroundColorectal cancer (CRC) is the third most common cancer type and one of the leading causes of cancer-related death worldwide. The treatment of advanced metastatic CRC relies on classical chemotherapy combinations (5-fluorouracil, oxaliplatin or irinotecan). However, their use is limited by...
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| Published in: | Journal for immunotherapy of cancer Vol. 13; no. 3; p. e010791 |
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| Main Authors: | , , , , , , , , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
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BMJ Publishing Group Ltd
26.03.2025
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| ISSN: | 2051-1426, 2051-1426 |
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| Abstract | BackgroundColorectal cancer (CRC) is the third most common cancer type and one of the leading causes of cancer-related death worldwide. The treatment of advanced metastatic CRC relies on classical chemotherapy combinations (5-fluorouracil, oxaliplatin or irinotecan). However, their use is limited by the emergence of resistance mechanisms, including to oxaliplatin. In this context, we recently showed that the combination of oxaliplatin and ataxia telangiectasia and Rad3-related protein inhibition (VE-822) is synergistic and may have a potential therapeutic effect in metastatic CRC management.MethodsIn this study, we investigated the role of the VE-822+oxaliplatin (Vox) combination on the immune response and its potential synergy with an anti-programmed-cell Death receptor-1 (PD-1) antibody. We used cell lines and organoids from metastatic CRC to investigate in vitro Vox efficacy and orthotopic syngeneic mouse models of metastatic CRC to assess the efficacy of Vox+anti-PD-1 antibody and identify the involved immune cells.ResultsThe Vox+anti-PD-1 antibody combination completely cured tumor-bearing mice and protected them from a rechallenge. Vox was associated with a reduction of tumor-infiltrated neutrophils, CD206+ macrophages and regulatory T cells. Vox also induced a deep depletion of blood neutrophils. The increased bone marrow granulopoiesis failed to compensate for the Vox-mediated mature neutrophil depletion. Neutrophil depletion using a mouse recombinant anti-Ly6G antibody partially mimicked the Vox effect on the tumor microenvironment, but to a lower extent compared with the Vox+anti-PD-1 antibody combination. Vox, but not neutrophil depletion, led to the emergence of an Ly6C+ PD-1+ CD8+ T-cell population in the blood and spleen of tumor-harboring mice. These cells were proliferating, and expressed IFN-γ, CD62L, CXCR3 and Eomes. Moreover, the proportion of tumor antigen-specific T cells and of CD122+ BCL6+ T cells, which shared phenotypic characteristics with stem-like CD8+ T cells, was increased in treated mice.ConclusionsOur work strongly suggests that the Vox+anti-PD-1 antibody combination might significantly improve survival in patients with metastatic and treatment-refractory CRC by acting both on cancer cells and CD8+ T cells. |
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| AbstractList | BackgroundColorectal cancer (CRC) is the third most common cancer type and one of the leading causes of cancer-related death worldwide. The treatment of advanced metastatic CRC relies on classical chemotherapy combinations (5-fluorouracil, oxaliplatin or irinotecan). However, their use is limited by the emergence of resistance mechanisms, including to oxaliplatin. In this context, we recently showed that the combination of oxaliplatin and ataxia telangiectasia and Rad3-related protein inhibition (VE-822) is synergistic and may have a potential therapeutic effect in metastatic CRC management.MethodsIn this study, we investigated the role of the VE-822+oxaliplatin (Vox) combination on the immune response and its potential synergy with an anti-programmed-cell Death receptor-1 (PD-1) antibody. We used cell lines and organoids from metastatic CRC to investigate in vitro Vox efficacy and orthotopic syngeneic mouse models of metastatic CRC to assess the efficacy of Vox+anti-PD-1 antibody and identify the involved immune cells.ResultsThe Vox+anti-PD-1 antibody combination completely cured tumor-bearing mice and protected them from a rechallenge. Vox was associated with a reduction of tumor-infiltrated neutrophils, CD206+ macrophages and regulatory T cells. Vox also induced a deep depletion of blood neutrophils. The increased bone marrow granulopoiesis failed to compensate for the Vox-mediated mature neutrophil depletion. Neutrophil depletion using a mouse recombinant anti-Ly6G antibody partially mimicked the Vox effect on the tumor microenvironment, but to a lower extent compared with the Vox+anti-PD-1 antibody combination. Vox, but not neutrophil depletion, led to the emergence of an Ly6C+ PD-1+ CD8+ T-cell population in the blood and spleen of tumor-harboring mice. These cells were proliferating, and expressed IFN-γ, CD62L, CXCR3 and Eomes. Moreover, the proportion of tumor antigen-specific T cells and of CD122+ BCL6+ T cells, which shared phenotypic characteristics with stem-like CD8+ T cells, was increased in treated mice.ConclusionsOur work strongly suggests that the Vox+anti-PD-1 antibody combination might significantly improve survival in patients with metastatic and treatment-refractory CRC by acting both on cancer cells and CD8+ T cells. Colorectal cancer (CRC) is the third most common cancer type and one of the leading causes of cancer-related death worldwide. The treatment of advanced metastatic CRC relies on classical chemotherapy combinations (5-fluorouracil, oxaliplatin or irinotecan). However, their use is limited by the emergence of resistance mechanisms, including to oxaliplatin. In this context, we recently showed that the combination of oxaliplatin and ataxia telangiectasia and Rad3-related protein inhibition (VE-822) is synergistic and may have a potential therapeutic effect in metastatic CRC management.BACKGROUNDColorectal cancer (CRC) is the third most common cancer type and one of the leading causes of cancer-related death worldwide. The treatment of advanced metastatic CRC relies on classical chemotherapy combinations (5-fluorouracil, oxaliplatin or irinotecan). However, their use is limited by the emergence of resistance mechanisms, including to oxaliplatin. In this context, we recently showed that the combination of oxaliplatin and ataxia telangiectasia and Rad3-related protein inhibition (VE-822) is synergistic and may have a potential therapeutic effect in metastatic CRC management.In this study, we investigated the role of the VE-822+oxaliplatin (Vox) combination on the immune response and its potential synergy with an anti-programmed-cell Death receptor-1 (PD-1) antibody. We used cell lines and organoids from metastatic CRC to investigate in vitro Vox efficacy and orthotopic syngeneic mouse models of metastatic CRC to assess the efficacy of Vox+anti-PD-1 antibody and identify the involved immune cells.METHODSIn this study, we investigated the role of the VE-822+oxaliplatin (Vox) combination on the immune response and its potential synergy with an anti-programmed-cell Death receptor-1 (PD-1) antibody. We used cell lines and organoids from metastatic CRC to investigate in vitro Vox efficacy and orthotopic syngeneic mouse models of metastatic CRC to assess the efficacy of Vox+anti-PD-1 antibody and identify the involved immune cells.The Vox+anti-PD-1 antibody combination completely cured tumor-bearing mice and protected them from a rechallenge. Vox was associated with a reduction of tumor-infiltrated neutrophils, CD206+ macrophages and regulatory T cells. Vox also induced a deep depletion of blood neutrophils. The increased bone marrow granulopoiesis failed to compensate for the Vox-mediated mature neutrophil depletion. Neutrophil depletion using a mouse recombinant anti-Ly6G antibody partially mimicked the Vox effect on the tumor microenvironment, but to a lower extent compared with the Vox+anti-PD-1 antibody combination. Vox, but not neutrophil depletion, led to the emergence of an Ly6C+ PD-1+ CD8+ T-cell population in the blood and spleen of tumor-harboring mice. These cells were proliferating, and expressed IFN-γ, CD62L, CXCR3 and Eomes. Moreover, the proportion of tumor antigen-specific T cells and of CD122+ BCL6+ T cells, which shared phenotypic characteristics with stem-like CD8+ T cells, was increased in treated mice.RESULTSThe Vox+anti-PD-1 antibody combination completely cured tumor-bearing mice and protected them from a rechallenge. Vox was associated with a reduction of tumor-infiltrated neutrophils, CD206+ macrophages and regulatory T cells. Vox also induced a deep depletion of blood neutrophils. The increased bone marrow granulopoiesis failed to compensate for the Vox-mediated mature neutrophil depletion. Neutrophil depletion using a mouse recombinant anti-Ly6G antibody partially mimicked the Vox effect on the tumor microenvironment, but to a lower extent compared with the Vox+anti-PD-1 antibody combination. Vox, but not neutrophil depletion, led to the emergence of an Ly6C+ PD-1+ CD8+ T-cell population in the blood and spleen of tumor-harboring mice. These cells were proliferating, and expressed IFN-γ, CD62L, CXCR3 and Eomes. Moreover, the proportion of tumor antigen-specific T cells and of CD122+ BCL6+ T cells, which shared phenotypic characteristics with stem-like CD8+ T cells, was increased in treated mice.Our work strongly suggests that the Vox+anti-PD-1 antibody combination might significantly improve survival in patients with metastatic and treatment-refractory CRC by acting both on cancer cells and CD8+ T cells.CONCLUSIONSOur work strongly suggests that the Vox+anti-PD-1 antibody combination might significantly improve survival in patients with metastatic and treatment-refractory CRC by acting both on cancer cells and CD8+ T cells. Background Colorectal cancer (CRC) is the third most common cancer type and one of the leading causes of cancer-related death worldwide. The treatment of advanced metastatic CRC relies on classical chemotherapy combinations (5-fluorouracil, oxaliplatin or irinotecan). However, their use is limited by the emergence of resistance mechanisms, including to oxaliplatin. In this context, we recently showed that the combination of oxaliplatin and ataxia telangiectasia and Rad3-related protein inhibition (VE-822) is synergistic and may have a potential therapeutic effect in metastatic CRC management.Methods In this study, we investigated the role of the VE-822+oxaliplatin (Vox) combination on the immune response and its potential synergy with an anti-programmed-cell Death receptor-1 (PD-1) antibody. We used cell lines and organoids from metastatic CRC to investigate in vitro Vox efficacy and orthotopic syngeneic mouse models of metastatic CRC to assess the efficacy of Vox+anti-PD-1 antibody and identify the involved immune cells.Results The Vox+anti-PD-1 antibody combination completely cured tumor-bearing mice and protected them from a rechallenge. Vox was associated with a reduction of tumor-infiltrated neutrophils, CD206+ macrophages and regulatory T cells. Vox also induced a deep depletion of blood neutrophils. The increased bone marrow granulopoiesis failed to compensate for the Vox-mediated mature neutrophil depletion. Neutrophil depletion using a mouse recombinant anti-Ly6G antibody partially mimicked the Vox effect on the tumor microenvironment, but to a lower extent compared with the Vox+anti-PD-1 antibody combination. Vox, but not neutrophil depletion, led to the emergence of an Ly6C+ PD-1+ CD8+ T-cell population in the blood and spleen of tumor-harboring mice. These cells were proliferating, and expressed IFN-γ, CD62L, CXCR3 and Eomes. Moreover, the proportion of tumor antigen-specific T cells and of CD122+ BCL6+ T cells, which shared phenotypic characteristics with stem-like CD8+ T cells, was increased in treated mice.Conclusions Our work strongly suggests that the Vox+anti-PD-1 antibody combination might significantly improve survival in patients with metastatic and treatment-refractory CRC by acting both on cancer cells and CD8+ T cells. Colorectal cancer (CRC) is the third most common cancer type and one of the leading causes of cancer-related death worldwide. The treatment of advanced metastatic CRC relies on classical chemotherapy combinations (5-fluorouracil, oxaliplatin or irinotecan). However, their use is limited by the emergence of resistance mechanisms, including to oxaliplatin. In this context, we recently showed that the combination of oxaliplatin and ataxia telangiectasia and Rad3-related protein inhibition (VE-822) is synergistic and may have a potential therapeutic effect in metastatic CRC management. In this study, we investigated the role of the VE-822+oxaliplatin (Vox) combination on the immune response and its potential synergy with an anti-programmed-cell Death receptor-1 (PD-1) antibody. We used cell lines and organoids from metastatic CRC to investigate in vitro Vox efficacy and orthotopic syngeneic mouse models of metastatic CRC to assess the efficacy of Vox+anti-PD-1 antibody and identify the involved immune cells. The Vox+anti-PD-1 antibody combination completely cured tumor-bearing mice and protected them from a rechallenge. Vox was associated with a reduction of tumor-infiltrated neutrophils, CD206 macrophages and regulatory T cells. Vox also induced a deep depletion of blood neutrophils. The increased bone marrow granulopoiesis failed to compensate for the Vox-mediated mature neutrophil depletion. Neutrophil depletion using a mouse recombinant anti-Ly6G antibody partially mimicked the Vox effect on the tumor microenvironment, but to a lower extent compared with the Vox+anti-PD-1 antibody combination. Vox, but not neutrophil depletion, led to the emergence of an Ly6C PD-1 CD8 T-cell population in the blood and spleen of tumor-harboring mice. These cells were proliferating, and expressed IFN-γ, CD62L, CXCR3 and Eomes. Moreover, the proportion of tumor antigen-specific T cells and of CD122 BCL6 T cells, which shared phenotypic characteristics with stem-like CD8 T cells, was increased in treated mice. Our work strongly suggests that the Vox+anti-PD-1 antibody combination might significantly improve survival in patients with metastatic and treatment-refractory CRC by acting both on cancer cells and CD8 T cells. |
| Author | Quenet, François Jeanson, Laura Combes, Eve Lossaint, Gérald Gongora, Céline Faget, Julien Culerier, Elodie Andrade, Augusto Faria Milazzo, Louis-Antoine Marchive, Candice Fauvre, Alexandra Atis, Salima Bonnefoy, Nathalie Sgarbura, Olivia Corbeau, Ileana Ursino, Chiara Vezzio-Vié, Nadia Michaud, Henri-Alexandre Tosi, Diego Khellaf, Lakhdar Houede, Nadine Garambois, Veronique |
| Author_xml | – sequence: 1 givenname: Alexandra orcidid: 0009-0002-8967-7538 surname: Fauvre fullname: Fauvre, Alexandra organization: Résistance aux traitements et thérapies innovantes, Institut de Recherche en Cancérologie de Montpellier (IRCM), Université de Montpellier (UM), CNRS, Institut Régional du Cancer de Montpellier (ICM), Montpellier, France – sequence: 2 givenname: Chiara surname: Ursino fullname: Ursino, Chiara organization: Immunity and Cancer Team, Institut de Recherche en Cancérologie de Montpellier (IRCM), Université de Montpellier (UM), Institut Régional du Cancer de Montpellier (ICM), Montpellier, France – sequence: 3 givenname: Veronique surname: Garambois fullname: Garambois, Veronique organization: Résistance aux traitements et thérapies innovantes, Institut de Recherche en Cancérologie de Montpellier (IRCM), Université de Montpellier (UM), CNRS, Institut Régional du Cancer de Montpellier (ICM), Montpellier, France – sequence: 4 givenname: Elodie surname: Culerier fullname: Culerier, Elodie organization: Immunity and Cancer Team, Institut de Recherche en Cancérologie de Montpellier (IRCM), Université de Montpellier (UM), Institut Régional du Cancer de Montpellier (ICM), Montpellier, France – sequence: 5 givenname: Louis-Antoine orcidid: 0009-0004-8155-9021 surname: Milazzo fullname: Milazzo, Louis-Antoine organization: Résistance aux traitements et thérapies innovantes, Institut de Recherche en Cancérologie de Montpellier (IRCM), Université de Montpellier (UM), CNRS, Institut Régional du Cancer de Montpellier (ICM), Montpellier, France – sequence: 6 givenname: Nadia surname: Vezzio-Vié fullname: Vezzio-Vié, Nadia organization: Résistance aux traitements et thérapies innovantes, Institut de Recherche en Cancérologie de Montpellier (IRCM), Université de Montpellier (UM), CNRS, Institut Régional du Cancer de Montpellier (ICM), Montpellier, France – sequence: 7 givenname: Laura surname: Jeanson fullname: Jeanson, Laura organization: Résistance aux traitements et thérapies innovantes, Institut de Recherche en Cancérologie de Montpellier (IRCM), Université de Montpellier (UM), CNRS, Institut Régional du Cancer de Montpellier (ICM), Montpellier, France – sequence: 8 givenname: Candice surname: Marchive fullname: Marchive, Candice organization: Résistance aux traitements et thérapies innovantes, Institut de Recherche en Cancérologie de Montpellier (IRCM), Université de Montpellier (UM), CNRS, Institut Régional du Cancer de Montpellier (ICM), Montpellier, France – sequence: 9 givenname: Augusto Faria surname: Andrade fullname: Andrade, Augusto Faria organization: McGill University/Research Institute of McGill University, Nada Jabado Lab, Montreal, Quebec, Canada – sequence: 10 givenname: Eve orcidid: 0009-0001-7145-7599 surname: Combes fullname: Combes, Eve organization: Résistance aux traitements et thérapies innovantes, Institut de Recherche en Cancérologie de Montpellier (IRCM), Université de Montpellier (UM), CNRS, Institut Régional du Cancer de Montpellier (ICM), Montpellier, France – sequence: 11 givenname: Salima surname: Atis fullname: Atis, Salima organization: Résistance aux traitements et thérapies innovantes, Institut de Recherche en Cancérologie de Montpellier (IRCM), Université de Montpellier (UM), CNRS, Institut Régional du Cancer de Montpellier (ICM), Montpellier, France – sequence: 12 givenname: Gérald surname: Lossaint fullname: Lossaint, Gérald organization: Institut regional du Cancer de Montpellier, Montpellier, France – sequence: 13 givenname: François surname: Quenet fullname: Quenet, François organization: Institut regional du Cancer de Montpellier, Montpellier, France – sequence: 14 givenname: Henri-Alexandre orcidid: 0000-0002-6165-1929 surname: Michaud fullname: Michaud, Henri-Alexandre organization: Immunity and Cancer Team, Institut de Recherche en Cancérologie de Montpellier (IRCM), Université de Montpellier (UM), Institut Régional du Cancer de Montpellier (ICM), Montpellier, France – sequence: 15 givenname: Lakhdar surname: Khellaf fullname: Khellaf, Lakhdar organization: Department of Pathology, Montpellier University, Montpellier, France – sequence: 16 givenname: Ileana surname: Corbeau fullname: Corbeau, Ileana organization: Institut regional du Cancer de Montpellier, Montpellier, France – sequence: 17 givenname: Diego orcidid: 0000-0003-0401-7400 surname: Tosi fullname: Tosi, Diego organization: Medical Oncology Department, Institut régional du Cancer de Montpellier, Montpellier, France – sequence: 18 givenname: Nadine surname: Houede fullname: Houede, Nadine organization: Department of Oncology, University Hospital of Nimes, Nîmes, France – sequence: 19 givenname: Nathalie orcidid: 0000-0003-4814-6722 surname: Bonnefoy fullname: Bonnefoy, Nathalie organization: Immunity and Cancer Team, Institut de Recherche en Cancérologie de Montpellier (IRCM), Université de Montpellier (UM), Institut Régional du Cancer de Montpellier (ICM), Montpellier, France – sequence: 20 givenname: Olivia orcidid: 0000-0002-6965-3697 surname: Sgarbura fullname: Sgarbura, Olivia organization: Institut regional du Cancer de Montpellier, Montpellier, France – sequence: 21 givenname: Céline orcidid: 0000-0001-9034-4031 surname: Gongora fullname: Gongora, Céline email: celine.gongora@inserm.fr organization: CNRS, Paris, France – sequence: 22 givenname: Julien orcidid: 0000-0003-0848-7135 surname: Faget fullname: Faget, Julien email: julien.faget@inserm.fr organization: Immunity and Cancer Team, Institut de Recherche en Cancérologie de Montpellier (IRCM), Université de Montpellier (UM), Institut Régional du Cancer de Montpellier (ICM), Montpellier, France |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/40139833$$D View this record in MEDLINE/PubMed |
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| CitedBy_id | crossref_primary_10_3390_cancers17152593 |
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| Issue | 3 |
| Keywords | Colorectal Cancer Immune Checkpoint Inhibitor T cell Neutropenia |
| Language | English |
| License | This is an open access article distributed in accordance with the Creative Commons Attribution 4.0 Unported (CC BY 4.0) license, which permits others to copy, redistribute, remix, transform and build upon this work for any purpose, provided the original work is properly cited, a link to the licence is given, and indication of whether changes were made. See https://creativecommons.org/licenses/by/4.0/. Author(s) (or their employer(s)) 2025. Re-use permitted under CC BY. Published by BMJ Group. |
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| PublicationTitle | Journal for immunotherapy of cancer |
| PublicationTitleAbbrev | J Immunother Cancer |
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publication-title: Nat Commun doi: 10.1038/s41467-024-45996-4 – ident: 2025100300581516000_13.3.e010791.46 doi: 10.1038/s41591-024-02808-y – ident: 2025100300581516000_13.3.e010791.27 doi: 10.1016/j.ctrv.2017.11.007 – volume: 8 year: 2020 ident: 2025100300581516000_13.3.e010791.35 article-title: ATR inhibitor AZD6738 enhances the antitumor activity of radiotherapy and immune checkpoint inhibitors by potentiating the tumor immune microenvironment in hepatocellular carcinoma publication-title: J Immunother Cancer doi: 10.1136/jitc-2019-000340 – volume: 17 start-page: S41 year: 2022 ident: 2025100300581516000_13.3.e010791.19 article-title: OA15.05 HUDSON: An Open-Label, Multi-Drug, Biomarker-Directed Phase 2 Study in NSCLC Patients Who Progressed on Anti-PD-(L)1 Therapy publication-title: J Thorac Oncol doi: 10.1016/j.jtho.2022.07.074 – volume: 20 start-page: 442 year: 2021 ident: 2025100300581516000_13.3.e010791.10 article-title: Inhibition of indoleamine 2,3-dioxygenase 1 synergizes with oxaliplatin for efficient colorectal cancer therapy publication-title: Mol Ther Methods Clin Dev doi: 10.1016/j.omtm.2020.12.013 – volume: 3 start-page: 100554 year: 2022 ident: 2025100300581516000_13.3.e010791.42 article-title: AXL targeting restores PD-1 blockade sensitivity of STK11/LKB1 mutant NSCLC through expansion of TCF1+ CD8 T cells publication-title: Cell Reports Medicine doi: 10.1016/j.xcrm.2022.100554 – ident: 2025100300581516000_13.3.e010791.31 doi: 10.1016/j.cell.2013.04.040 – ident: 2025100300581516000_13.3.e010791.38 doi: 10.1093/carcin/bgx002 – volume: 17 year: 2016 ident: 2025100300581516000_13.3.e010791.29 article-title: The Role of Chemokines in Promoting Colorectal Cancer Invasion/Metastasis publication-title: Int J Mol Sci doi: 10.3390/ijms17050643 – volume: 73 year: 2024 ident: 2025100300581516000_13.3.e010791.8 article-title: Immunogenic cell death in colorectal cancer: a review of mechanisms and clinical utility publication-title: Cancer Immunol Immunother 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| Snippet | BackgroundColorectal cancer (CRC) is the third most common cancer type and one of the leading causes of cancer-related death worldwide. The treatment of... Colorectal cancer (CRC) is the third most common cancer type and one of the leading causes of cancer-related death worldwide. The treatment of advanced... Background Colorectal cancer (CRC) is the third most common cancer type and one of the leading causes of cancer-related death worldwide. The treatment of... |
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| SubjectTerms | Animals Antibodies Antineoplastic Combined Chemotherapy Protocols - pharmacology Antineoplastic Combined Chemotherapy Protocols - therapeutic use Ataxia Basic and translational cancer immunology Bioluminescence Cancer therapies Cell death Cell Line, Tumor Chemotherapy Clinical trials Colonic Neoplasms - drug therapy Colonic Neoplasms - immunology Colonic Neoplasms - pathology Colorectal Cancer Female Gastric cancer Humans Immune Checkpoint Inhibitor Immune checkpoint inhibitors Immune Checkpoint Inhibitors - pharmacology Immunotherapy Kinases Lymphocytes Metastasis Mice Neutropenia Neutrophils Oxaliplatin - pharmacology Oxaliplatin - therapeutic use Patients Penicillin Programmed Cell Death 1 Receptor - antagonists & inhibitors T cell Tumors |
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| Title | Oxaliplatin, ATR inhibitor and anti-PD-1 antibody combination therapy controls colon carcinoma growth, induces local and systemic changes in the immune compartment, and protects against tumor rechallenge in mice |
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