Irradiated tumor cell-derived microparticles mediate tumor eradication via cell killing and immune reprogramming

Radiotherapy (RT) is routinely used in cancer treatment, but expansion of its clinical indications remains challenging. The mechanism underlying the radiation-induced bystander effect (RIBE) is not understood and not therapeutically exploited. We suggest that the RIBE is predominantly mediated by ir...

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Published inScience advances Vol. 6; no. 13; p. eaay9789
Main Authors Wan, Chao, Sun, Yajie, Tian, Yu, Lu, Lisen, Dai, Xiaomeng, Meng, Jingshu, Huang, Jing, He, Qianyuan, Wu, Bian, Zhang, Zhanjie, Jiang, Ke, Hu, Desheng, Wu, Gang, Lovell, Jonathan F, Jin, Honglin, Yang, Kunyu
Format Journal Article
LanguageEnglish
Published United States American Association for the Advancement of Science 01.03.2020
Subjects
Cancer
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Abstract Radiotherapy (RT) is routinely used in cancer treatment, but expansion of its clinical indications remains challenging. The mechanism underlying the radiation-induced bystander effect (RIBE) is not understood and not therapeutically exploited. We suggest that the RIBE is predominantly mediated by irradiated tumor cell-released microparticles (RT-MPs), which induce broad antitumor effects and cause immunogenic death mainly through ferroptosis. Using a mouse model of malignant pleural effusion (MPE), we demonstrated that RT-MPs polarized microenvironmental M2 tumor-associated macrophages (M2-TAMs) to M1-TAMs and modulated antitumor interactions between TAMs and tumor cells. Following internalization of RT-MPs, TAMs displayed increased programmed cell death ligand 1 (PD-L1) expression, enhancing follow-up combined anti-PD-1 therapy that confers an ablative effect against MPE and cisplatin-resistant MPE mouse models. Immunological memory effects were induced.
AbstractList By mimicking the RIBE machinery, we provided an indirect radiotherapy approach based on RT-MP for eradication of MPE in mice. Radiotherapy (RT) is routinely used in cancer treatment, but expansion of its clinical indications remains challenging. The mechanism underlying the radiation-induced bystander effect (RIBE) is not understood and not therapeutically exploited. We suggest that the RIBE is predominantly mediated by irradiated tumor cell–released microparticles (RT-MPs), which induce broad antitumor effects and cause immunogenic death mainly through ferroptosis. Using a mouse model of malignant pleural effusion (MPE), we demonstrated that RT-MPs polarized microenvironmental M2 tumor-associated macrophages (M2-TAMs) to M1-TAMs and modulated antitumor interactions between TAMs and tumor cells. Following internalization of RT-MPs, TAMs displayed increased programmed cell death ligand 1 (PD-L1) expression, enhancing follow-up combined anti–PD-1 therapy that confers an ablative effect against MPE and cisplatin-resistant MPE mouse models. Immunological memory effects were induced.
Radiotherapy (RT) is routinely used in cancer treatment, but expansion of its clinical indications remains challenging. The mechanism underlying the radiation-induced bystander effect (RIBE) is not understood and not therapeutically exploited. We suggest that the RIBE is predominantly mediated by irradiated tumor cell-released microparticles (RT-MPs), which induce broad antitumor effects and cause immunogenic death mainly through ferroptosis. Using a mouse model of malignant pleural effusion (MPE), we demonstrated that RT-MPs polarized microenvironmental M2 tumor-associated macrophages (M2-TAMs) to M1-TAMs and modulated antitumor interactions between TAMs and tumor cells. Following internalization of RT-MPs, TAMs displayed increased programmed cell death ligand 1 (PD-L1) expression, enhancing follow-up combined anti-PD-1 therapy that confers an ablative effect against MPE and cisplatin-resistant MPE mouse models. Immunological memory effects were induced.
Author Sun, Yajie
He, Qianyuan
Jin, Honglin
Lu, Lisen
Tian, Yu
Yang, Kunyu
Wu, Bian
Wan, Chao
Meng, Jingshu
Dai, Xiaomeng
Hu, Desheng
Huang, Jing
Zhang, Zhanjie
Wu, Gang
Jiang, Ke
Lovell, Jonathan F
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  orcidid: 0000-0001-9608-6483
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– sequence: 7
  givenname: Jing
  surname: Huang
  fullname: Huang, Jing
  organization: Cancer Center, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, China
– sequence: 8
  givenname: Qianyuan
  orcidid: 0000-0003-3504-0961
  surname: He
  fullname: He, Qianyuan
  organization: Cancer Center, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, China
– sequence: 9
  givenname: Bian
  surname: Wu
  fullname: Wu, Bian
  organization: Cancer Center, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, China
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  givenname: Zhanjie
  surname: Zhang
  fullname: Zhang, Zhanjie
  organization: Cancer Center, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, China
– sequence: 11
  givenname: Ke
  surname: Jiang
  fullname: Jiang, Ke
  organization: Department of Thoracic Surgery, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
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  givenname: Desheng
  surname: Hu
  fullname: Hu, Desheng
  organization: Department of Integrated Traditional Chinese and Western Medicine, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China
– sequence: 13
  givenname: Gang
  surname: Wu
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  organization: Cancer Center, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, China
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  givenname: Jonathan F
  orcidid: 0000-0002-9052-884X
  surname: Lovell
  fullname: Lovell, Jonathan F
  organization: Department of Chemical and Biological Engineering, University at Buffalo, State University of New York. Buffalo, NY 14260, USA
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  givenname: Honglin
  orcidid: 0000-0002-4398-9539
  surname: Jin
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  organization: Cancer Center, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, China
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  givenname: Kunyu
  orcidid: 0000-0002-2575-4736
  surname: Yang
  fullname: Yang, Kunyu
  organization: Cancer Center, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, China
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Snippet Radiotherapy (RT) is routinely used in cancer treatment, but expansion of its clinical indications remains challenging. The mechanism underlying the...
By mimicking the RIBE machinery, we provided an indirect radiotherapy approach based on RT-MP for eradication of MPE in mice. Radiotherapy (RT) is routinely...
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Title Irradiated tumor cell-derived microparticles mediate tumor eradication via cell killing and immune reprogramming
URI https://www.ncbi.nlm.nih.gov/pubmed/32232155
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https://pubmed.ncbi.nlm.nih.gov/PMC7096163
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