PD-1 blockade and OX40 triggering synergistically protects against tumor growth in a murine model of ovarian cancer.

The co-inhibitory receptor Programmed Death-1 (PD-1) curtails immune responses and prevent autoimmunity, however, tumors exploit this pathway to escape from immune destruction. The co-stimulatory receptor OX40 is upregulated on T cells following activation and increases their clonal expansion, survi...

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Main Authors: Zhiqiang Guo, Xin Wang, Dali Cheng, Zhijun Xia, Meng Luan, Shulan Zhang
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2014-01-01
Series:PLoS ONE
Online Access:https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0089350&type=printable
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author Zhiqiang Guo
Xin Wang
Dali Cheng
Zhijun Xia
Meng Luan
Shulan Zhang
author_facet Zhiqiang Guo
Xin Wang
Dali Cheng
Zhijun Xia
Meng Luan
Shulan Zhang
author_sort Zhiqiang Guo
collection DOAJ
description The co-inhibitory receptor Programmed Death-1 (PD-1) curtails immune responses and prevent autoimmunity, however, tumors exploit this pathway to escape from immune destruction. The co-stimulatory receptor OX40 is upregulated on T cells following activation and increases their clonal expansion, survival and cytokine production when engaged. Although antagonistic anti-PD-1 or agonistic anti-OX40 antibodies can promote the rejection of several murine tumors, some poorly immunogenic tumors were refractory to this treatment. In the present study, we evaluated the antitumor effects and mechanisms of combinatorial PD-1 blockade and OX40 triggering in a murine ID8 ovarian cancer model. Although individual anti-PD-1 or OX40 mAb treatment was ineffective in tumor protection against 10-day established ID8 tumor, combined anti-PD-1/OX40 mAb treatment markedly inhibited tumor outgrowth with 60% of mice tumor free 90 days after tumor inoculation. Tumor protection was associated with a systemic immune response with memory and antigen specificity and required CD4(+) cells and CD8(+) T cells. The anti-PD-1/OX40 mAb treatment increased CD4(+) and CD8(+) cells and decreased immunosuppressive CD4(+)FoxP3(+) regulatory T (Treg) cells and CD11b(+)Gr-1(+) myeloid suppressor cells (MDSC), giving rise to significantly higher ratios of both effector CD4(+) and CD8(+) cells to Treg and MDSC in peritoneal cavity; Quantitative RT-PCR data further demonstrated the induction of a local immunostimulatory milieu by anti-PD-1/OX40 mAb treatment. The splenic CD8(+) T cells from combined mAb treated mice produced high levels of IFN-γ upon tumor antigen stimulation and exhibited antigen-specific cytolytic activity. To our knowledge, this is the first study testing the antitumor effects of combined anti-PD-1/OX40 mAb in a murine ovarian cancer model, and our results provide a rationale for clinical trials evaluating ovarian cancer immunotherapy using this combination of mAb.
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spelling doaj-art-a27d2b76b1be46a2b77b87c82ed633cd2025-08-20T02:15:19ZengPublic Library of Science (PLoS)PLoS ONE1932-62032014-01-0192e8935010.1371/journal.pone.0089350PD-1 blockade and OX40 triggering synergistically protects against tumor growth in a murine model of ovarian cancer.Zhiqiang GuoXin WangDali ChengZhijun XiaMeng LuanShulan ZhangThe co-inhibitory receptor Programmed Death-1 (PD-1) curtails immune responses and prevent autoimmunity, however, tumors exploit this pathway to escape from immune destruction. The co-stimulatory receptor OX40 is upregulated on T cells following activation and increases their clonal expansion, survival and cytokine production when engaged. Although antagonistic anti-PD-1 or agonistic anti-OX40 antibodies can promote the rejection of several murine tumors, some poorly immunogenic tumors were refractory to this treatment. In the present study, we evaluated the antitumor effects and mechanisms of combinatorial PD-1 blockade and OX40 triggering in a murine ID8 ovarian cancer model. Although individual anti-PD-1 or OX40 mAb treatment was ineffective in tumor protection against 10-day established ID8 tumor, combined anti-PD-1/OX40 mAb treatment markedly inhibited tumor outgrowth with 60% of mice tumor free 90 days after tumor inoculation. Tumor protection was associated with a systemic immune response with memory and antigen specificity and required CD4(+) cells and CD8(+) T cells. The anti-PD-1/OX40 mAb treatment increased CD4(+) and CD8(+) cells and decreased immunosuppressive CD4(+)FoxP3(+) regulatory T (Treg) cells and CD11b(+)Gr-1(+) myeloid suppressor cells (MDSC), giving rise to significantly higher ratios of both effector CD4(+) and CD8(+) cells to Treg and MDSC in peritoneal cavity; Quantitative RT-PCR data further demonstrated the induction of a local immunostimulatory milieu by anti-PD-1/OX40 mAb treatment. The splenic CD8(+) T cells from combined mAb treated mice produced high levels of IFN-γ upon tumor antigen stimulation and exhibited antigen-specific cytolytic activity. To our knowledge, this is the first study testing the antitumor effects of combined anti-PD-1/OX40 mAb in a murine ovarian cancer model, and our results provide a rationale for clinical trials evaluating ovarian cancer immunotherapy using this combination of mAb.https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0089350&type=printable
spellingShingle Zhiqiang Guo
Xin Wang
Dali Cheng
Zhijun Xia
Meng Luan
Shulan Zhang
PD-1 blockade and OX40 triggering synergistically protects against tumor growth in a murine model of ovarian cancer.
PLoS ONE
title PD-1 blockade and OX40 triggering synergistically protects against tumor growth in a murine model of ovarian cancer.
title_full PD-1 blockade and OX40 triggering synergistically protects against tumor growth in a murine model of ovarian cancer.
title_fullStr PD-1 blockade and OX40 triggering synergistically protects against tumor growth in a murine model of ovarian cancer.
title_full_unstemmed PD-1 blockade and OX40 triggering synergistically protects against tumor growth in a murine model of ovarian cancer.
title_short PD-1 blockade and OX40 triggering synergistically protects against tumor growth in a murine model of ovarian cancer.
title_sort pd 1 blockade and ox40 triggering synergistically protects against tumor growth in a murine model of ovarian cancer
url https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0089350&type=printable
work_keys_str_mv AT zhiqiangguo pd1blockadeandox40triggeringsynergisticallyprotectsagainsttumorgrowthinamurinemodelofovariancancer
AT xinwang pd1blockadeandox40triggeringsynergisticallyprotectsagainsttumorgrowthinamurinemodelofovariancancer
AT dalicheng pd1blockadeandox40triggeringsynergisticallyprotectsagainsttumorgrowthinamurinemodelofovariancancer
AT zhijunxia pd1blockadeandox40triggeringsynergisticallyprotectsagainsttumorgrowthinamurinemodelofovariancancer
AT mengluan pd1blockadeandox40triggeringsynergisticallyprotectsagainsttumorgrowthinamurinemodelofovariancancer
AT shulanzhang pd1blockadeandox40triggeringsynergisticallyprotectsagainsttumorgrowthinamurinemodelofovariancancer