Neutrophil-activating therapy for the treatment of cancer
Despite their cytotoxic capacity, neutrophils are often co-opted by cancers to promote immunosuppression, tumor growth, and metastasis. Consequently, these cells have received little attention as potential cancer immunotherapeutic agents. Here, we demonstrate in mouse models that neutrophils can be...
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| Published in | Cancer cell Vol. 41; no. 2; pp. 356 - 372.e10 |
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| Main Authors | , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
13.02.2023
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Despite their cytotoxic capacity, neutrophils are often co-opted by cancers to promote immunosuppression, tumor growth, and metastasis. Consequently, these cells have received little attention as potential cancer immunotherapeutic agents. Here, we demonstrate in mouse models that neutrophils can be harnessed to induce eradication of tumors and reduce metastatic seeding through the combined actions of tumor necrosis factor, CD40 agonist, and tumor-binding antibody. The same combination activates human neutrophils in vitro, enabling their lysis of human tumor cells. Mechanistically, this therapy induces rapid mobilization and tumor infiltration of neutrophils along with complement activation in tumors. Complement component C5a activates neutrophils to produce leukotriene B4, which stimulates reactive oxygen species production via xanthine oxidase, resulting in oxidative damage and T cell-independent clearance of multiple tumor types. These data establish neutrophils as potent anti-tumor immune mediators and define an inflammatory pathway that can be harnessed to drive neutrophil-mediated eradication of cancer.
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•Therapeutically activated neutrophils infiltrate and eradicate multiple tumor types•Intratumoral TNF + anti-CD40 + anti-tumor antibodies induce an inflammatory cascade•Neutrophil C5AR1 signaling stimulates LTB4 release, driving ROS production via XO•Neutrophil-mediated oxidative damage drives T cell-independent tumor clearance
Linde et al. describe a cancer therapy that activates neutrophils to infiltrate and eradicate tumors and reduce metastatic seeding. The authors elucidate the responsible mechanism, which involves complement component C5a, leukotriene B4, and reactive oxygen species, and demonstrate the potential of harnessing neutrophils through inflammatory activation to drive tumor clearance. |
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| AbstractList | Despite their cytotoxic capacity, neutrophils are often co-opted by cancers to promote immunosuppression, tumor growth, and metastasis. Consequently, these cells have received little attention as potential cancer immunotherapeutic agents. Here, we demonstrate in mouse models that neutrophils can be harnessed to induce eradication of tumors and reduce metastatic seeding through the combined actions of tumor necrosis factor, CD40 agonist, and tumor-binding antibody. The same combination activates human neutrophils in vitro, enabling their lysis of human tumor cells. Mechanistically, this therapy induces rapid mobilization and tumor infiltration of neutrophils along with complement activation in tumors. Complement component C5a activates neutrophils to produce leukotriene B
, which stimulates reactive oxygen species production via xanthine oxidase, resulting in oxidative damage and T cell-independent clearance of multiple tumor types. These data establish neutrophils as potent anti-tumor immune mediators and define an inflammatory pathway that can be harnessed to drive neutrophil-mediated eradication of cancer. Despite their cytotoxic capacity, neutrophils are often co-opted by cancers to promote immunosuppression, tumor growth, and metastasis. Consequently, these cells have received little attention as potential cancer immunotherapeutic agents. Here, we demonstrate in mouse models that neutrophils can be harnessed to induce eradication of tumors and reduce metastatic seeding through the combined actions of tumor necrosis factor, CD40 agonist, and tumor-binding antibody. The same combination activates human neutrophils in vitro, enabling their lysis of human tumor cells. Mechanistically, this therapy induces rapid mobilization and tumor infiltration of neutrophils along with complement activation in tumors. Complement component C5a activates neutrophils to produce leukotriene B4, which stimulates reactive oxygen species production via xanthine oxidase, resulting in oxidative damage and T cell-independent clearance of multiple tumor types. These data establish neutrophils as potent anti-tumor immune mediators and define an inflammatory pathway that can be harnessed to drive neutrophil-mediated eradication of cancer.Despite their cytotoxic capacity, neutrophils are often co-opted by cancers to promote immunosuppression, tumor growth, and metastasis. Consequently, these cells have received little attention as potential cancer immunotherapeutic agents. Here, we demonstrate in mouse models that neutrophils can be harnessed to induce eradication of tumors and reduce metastatic seeding through the combined actions of tumor necrosis factor, CD40 agonist, and tumor-binding antibody. The same combination activates human neutrophils in vitro, enabling their lysis of human tumor cells. Mechanistically, this therapy induces rapid mobilization and tumor infiltration of neutrophils along with complement activation in tumors. Complement component C5a activates neutrophils to produce leukotriene B4, which stimulates reactive oxygen species production via xanthine oxidase, resulting in oxidative damage and T cell-independent clearance of multiple tumor types. These data establish neutrophils as potent anti-tumor immune mediators and define an inflammatory pathway that can be harnessed to drive neutrophil-mediated eradication of cancer. Despite their cytotoxic capacity, neutrophils are often co-opted by cancers to promote immunosuppression, tumor growth, and metastasis. Consequently, these cells have received little attention as potential cancer immunotherapeutic agents. Here, we demonstrate in mouse models that neutrophils can be harnessed to induce eradication of tumors and reduce metastatic seeding through the combined actions of tumor necrosis factor, CD40 agonist, and tumor-binding antibody. The same combination activates human neutrophils in vitro , enabling their lysis of human tumor cells. Mechanistically, this therapy induces rapid mobilization and tumor infiltration of neutrophils along with complement activation in tumors. Complement component C5a activates neutrophils to produce leukotriene B 4 , which stimulates reactive oxygen species production via xanthine oxidase, resulting in oxidative damage and T cell-independent clearance of multiple tumor types. These data establish neutrophils as potent anti-tumor immune mediators and define an inflammatory pathway that can be harnessed to drive neutrophil-mediated eradication of cancer. Linde et al. describe a cancer therapy that activates neutrophils to infiltrate and eradicate tumors and reduce metastatic seeding. The authors elucidate the responsible mechanism, which involves complement component C5a, leukotriene B 4 , and reactive oxygen species, and demonstrate the potential of harnessing neutrophils through inflammatory activation to drive tumor clearance. Despite their cytotoxic capacity, neutrophils are often co-opted by cancers to promote immunosuppression, tumor growth, and metastasis. Consequently, these cells have received little attention as potential cancer immunotherapeutic agents. Here, we demonstrate in mouse models that neutrophils can be harnessed to induce eradication of tumors and reduce metastatic seeding through the combined actions of tumor necrosis factor, CD40 agonist, and tumor-binding antibody. The same combination activates human neutrophils in vitro, enabling their lysis of human tumor cells. Mechanistically, this therapy induces rapid mobilization and tumor infiltration of neutrophils along with complement activation in tumors. Complement component C5a activates neutrophils to produce leukotriene B4, which stimulates reactive oxygen species production via xanthine oxidase, resulting in oxidative damage and T cell-independent clearance of multiple tumor types. These data establish neutrophils as potent anti-tumor immune mediators and define an inflammatory pathway that can be harnessed to drive neutrophil-mediated eradication of cancer. [Display omitted] •Therapeutically activated neutrophils infiltrate and eradicate multiple tumor types•Intratumoral TNF + anti-CD40 + anti-tumor antibodies induce an inflammatory cascade•Neutrophil C5AR1 signaling stimulates LTB4 release, driving ROS production via XO•Neutrophil-mediated oxidative damage drives T cell-independent tumor clearance Linde et al. describe a cancer therapy that activates neutrophils to infiltrate and eradicate tumors and reduce metastatic seeding. The authors elucidate the responsible mechanism, which involves complement component C5a, leukotriene B4, and reactive oxygen species, and demonstrate the potential of harnessing neutrophils through inflammatory activation to drive tumor clearance. |
| Author | Song, Wen-Chao Linde, Miles H. Zhang, Xiangyue Sheu, Lauren Y. Pilarowski, Genay Tolentino, Lorna L. Chiu, David Kung-Chun Qiu, Jingtao Van Deursen, Simon Shen, Lei Engleman, Edgar G. Prestwood, Tyler R. Reticker-Flynn, Nathan E. Linde, Ian L. |
| AuthorAffiliation | 2 Department of Pathology, Stanford University; Stanford, CA 94305, USA 4 Lead Contact 3 Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, The University of Pennsylvania; Philadelphia, PA 19104, USA 1 Program in Immunology, Stanford University; Stanford, CA 94305, USA |
| AuthorAffiliation_xml | – name: 2 Department of Pathology, Stanford University; Stanford, CA 94305, USA – name: 4 Lead Contact – name: 3 Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, The University of Pennsylvania; Philadelphia, PA 19104, USA – name: 1 Program in Immunology, Stanford University; Stanford, CA 94305, USA |
| Author_xml | – sequence: 1 givenname: Ian L. surname: Linde fullname: Linde, Ian L. organization: Program in Immunology, Stanford University, Stanford, CA 94305, USA – sequence: 2 givenname: Tyler R. surname: Prestwood fullname: Prestwood, Tyler R. organization: Department of Pathology, Stanford University, Stanford, CA 94305, USA – sequence: 3 givenname: Jingtao surname: Qiu fullname: Qiu, Jingtao organization: Department of Pathology, Stanford University, Stanford, CA 94305, USA – sequence: 4 givenname: Genay surname: Pilarowski fullname: Pilarowski, Genay organization: Department of Pathology, Stanford University, Stanford, CA 94305, USA – sequence: 5 givenname: Miles H. surname: Linde fullname: Linde, Miles H. organization: Program in Immunology, Stanford University, Stanford, CA 94305, USA – sequence: 6 givenname: Xiangyue surname: Zhang fullname: Zhang, Xiangyue organization: Department of Pathology, Stanford University, Stanford, CA 94305, USA – sequence: 7 givenname: Lei surname: Shen fullname: Shen, Lei organization: Department of Pathology, Stanford University, Stanford, CA 94305, USA – sequence: 8 givenname: Nathan E. surname: Reticker-Flynn fullname: Reticker-Flynn, Nathan E. organization: Department of Pathology, Stanford University, Stanford, CA 94305, USA – sequence: 9 givenname: David Kung-Chun surname: Chiu fullname: Chiu, David Kung-Chun organization: Department of Pathology, Stanford University, Stanford, CA 94305, USA – sequence: 10 givenname: Lauren Y. surname: Sheu fullname: Sheu, Lauren Y. organization: Department of Pathology, Stanford University, Stanford, CA 94305, USA – sequence: 11 givenname: Simon surname: Van Deursen fullname: Van Deursen, Simon organization: Department of Pathology, Stanford University, Stanford, CA 94305, USA – sequence: 12 givenname: Lorna L. surname: Tolentino fullname: Tolentino, Lorna L. organization: Department of Pathology, Stanford University, Stanford, CA 94305, USA – sequence: 13 givenname: Wen-Chao surname: Song fullname: Song, Wen-Chao organization: Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA – sequence: 14 givenname: Edgar G. surname: Engleman fullname: Engleman, Edgar G. email: edengleman@stanford.edu organization: Program in Immunology, Stanford University, Stanford, CA 94305, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/36706760$$D View this record in MEDLINE/PubMed |
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| Keywords | CD40 tumor immunology tumor necrosis factor cancer immunotherapy reactive oxygen species complement neutrophil xanthine oxidase C5a leukotriene B4 |
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| SubjectTerms | Animals Antineoplastic Agents C5a cancer immunotherapy CD40 complement Humans leukotriene B4 Leukotriene B4 - metabolism Leukotriene B4 - pharmacology Mice Neoplasms - drug therapy Neoplasms - metabolism neutrophil Neutrophils reactive oxygen species tumor immunology tumor necrosis factor Tumor Necrosis Factor-alpha - metabolism xanthine oxidase |
| Title | Neutrophil-activating therapy for the treatment of cancer |
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