PD-L1-mediated gasdermin C expression switches apoptosis to pyroptosis in cancer cells and facilitates tumour necrosis

Although pyroptosis is critical for macrophages against pathogen infection, its role and mechanism in cancer cells remains unclear. PD-L1 has been detected in the nucleus, with unknown function. Here we show that PD-L1 switches TNFα-induced apoptosis to pyroptosis in cancer cells, resulting in tumou...

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Published inNature cell biology Vol. 22; no. 10; pp. 1264 - 1275
Main Authors Hou, Junwei, Zhao, Rongce, Xia, Weiya, Chang, Chiung-Wen, You, Yun, Hsu, Jung-Mao, Nie, Lei, Chen, Yeh, Wang, Yu-Chuan, Liu, Chunxiao, Wang, Wei-Jan, Wu, Yun, Ke, Baozhen, Hsu, Jennifer L., Huang, Kebin, Ye, Zu, Yang, Yi, Xia, Xianghou, Li, Yintao, Li, Chia-Wei, Shao, Bin, Tainer, John A., Hung, Mien-Chie
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.10.2020
Nature Publishing Group
Subjects
13/1
13/106
13/51
631/67
631/80/82
64/60
Animals
Antibiotics
Apoptosis
B7-H1 Antigen - genetics
B7-H1 Antigen - metabolism
Biomarkers, Tumor - genetics
Biomarkers, Tumor - metabolism
Biomedical and Life Sciences
Breast cancer
Cancer
Cancer cells
Cancer Research
Caspase-8
Cell Biology
Cell membranes
Cell Proliferation
Cellular proteins
Chemotherapy
Developmental Biology
DNA-Binding Proteins - genetics
DNA-Binding Proteins - metabolism
Female
Gene expression
Gene Expression Regulation, Neoplastic
Genetic aspects
Health aspects
Humans
Hypoxia
Hypoxia - physiopathology
Immune checkpoint
Immunosuppressive agents
Inflammasomes
Life Sciences
Macrophages
Mice
Mice, Inbred BALB C
Mice, Nude
Necrosis
Neoplasms - genetics
Neoplasms - metabolism
Neoplasms - pathology
Nuclear transport
Nuclei (cytology)
PD-L1 protein
Pyroptosis
Stat3 protein
Stem Cells
Switches
Transcription
Translocation
Tumor Cells, Cultured
Tumor necrosis factor-α
Tumor-Associated Macrophages
Tumors
Xenograft Model Antitumor Assays
United States
Online AccessGet full text

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Abstract Although pyroptosis is critical for macrophages against pathogen infection, its role and mechanism in cancer cells remains unclear. PD-L1 has been detected in the nucleus, with unknown function. Here we show that PD-L1 switches TNFα-induced apoptosis to pyroptosis in cancer cells, resulting in tumour necrosis. Under hypoxia, p-Stat3 physically interacts with PD-L1 and facilitates its nuclear translocation, enhancing the transcription of the gasdermin C ( GSDMC ) gene. GSDMC is specifically cleaved by caspase-8 with TNFα treatment, generating a GSDMC N-terminal domain that forms pores on the cell membrane and induces pyroptosis. Nuclear PD-L1, caspase-8 and GSDMC are required for macrophage-derived TNFα-induced tumour necrosis in vivo. Moreover, high expression of GSDMC correlates with poor survival. Antibiotic chemotherapy drugs induce pyroptosis in breast cancer. These findings identify a non-immune checkpoint function of PD-L1 and provide an unexpected concept that GSDMC/caspase-8 mediates a non-canonical pyroptosis pathway in cancer cells, causing tumour necrosis. Hou et al. show that following hypoxia PD-L1 translocates into the nucleus to enhance transcription of GSDMC, which is then cleaved and activated by caspase-8 to cause pyroptosis in cancer cells.
AbstractList Although pyroptosis is critical for macrophages against pathogen infection, its role and mechanism in cancer cells remains unclear. PD-L1 has been detected in the nucleus, with unknown function. Here we show that PD-L1 switches TNFα-induced apoptosis to pyroptosis in cancer cells, resulting in tumour necrosis. Under hypoxia, p-Stat3 physically interacts with PD-L1 and facilitates its nuclear translocation, enhancing the transcription of the gasdermin C (GSDMC) gene. GSDMC is specifically cleaved by caspase-8 with TNFα treatment, generating a GSDMC N-terminal domain that forms pores on the cell membrane and induces pyroptosis. Nuclear PD-L1, caspase-8 and GSDMC are required for macrophage-derived TNFα-induced tumour necrosis in vivo. Moreover, high expression of GSDMC correlates with poor survival. Antibiotic chemotherapy drugs induce pyroptosis in breast cancer. These findings identify a non-immune checkpoint function of PD-L1 and provide an unexpected concept that GSDMC/caspase-8 mediates a non-canonical pyroptosis pathway in cancer cells, causing tumour necrosis.Although pyroptosis is critical for macrophages against pathogen infection, its role and mechanism in cancer cells remains unclear. PD-L1 has been detected in the nucleus, with unknown function. Here we show that PD-L1 switches TNFα-induced apoptosis to pyroptosis in cancer cells, resulting in tumour necrosis. Under hypoxia, p-Stat3 physically interacts with PD-L1 and facilitates its nuclear translocation, enhancing the transcription of the gasdermin C (GSDMC) gene. GSDMC is specifically cleaved by caspase-8 with TNFα treatment, generating a GSDMC N-terminal domain that forms pores on the cell membrane and induces pyroptosis. Nuclear PD-L1, caspase-8 and GSDMC are required for macrophage-derived TNFα-induced tumour necrosis in vivo. Moreover, high expression of GSDMC correlates with poor survival. Antibiotic chemotherapy drugs induce pyroptosis in breast cancer. These findings identify a non-immune checkpoint function of PD-L1 and provide an unexpected concept that GSDMC/caspase-8 mediates a non-canonical pyroptosis pathway in cancer cells, causing tumour necrosis.
Pyroptosis is critical for macrophages against pathogen infection, but its role and mechanism in cancer cells remain unclear. PD-L1 has been detected in the nucleus with unknown function. Here, we show that PD-L1 switches TNFα-induced apoptosis to pyroptosis in cancer cells, resulting in tumor necrosis. Under hypoxia, p-Stat3 physically interacts with PD-L1 and facilitates its nuclear translocation, enhancing gasdermin C (GSDMC) gene transcription. GSDMC is specifically cleaved by caspase-8 with TNFα treatment, generating a GSDMC N-terminal domain that forms pores on cell membrane and induces pyroptosis. Nuclear PD-L1, caspase-8, and GSDMC are required for macrophage-derived TNFα-induced tumor necrosis in vivo . Moreover, high expression of GSDMC correlates with poor survival. Antibiotic chemotherapy drugs induce pyroptosis in breast cancer. These findings identify a non-immune checkpoint function of PD-L1 and provide an unexpected concept that GSDMC/Caspas-8 mediates non-canonical pyroptosis pathway in cancer cells, causing tumor necrosis.
Although pyroptosis is critical for macrophages against pathogen infection, its role and mechanism in cancer cells remains unclear. PD-L1 has been detected in the nucleus, with unknown function. Here we show that PD-L1 switches TNFα-induced apoptosis to pyroptosis in cancer cells, resulting in tumour necrosis. Under hypoxia, p-Stat3 physically interacts with PD-L1 and facilitates its nuclear translocation, enhancing the transcription of the gasdermin C (GSDMC) gene. GSDMC is specifically cleaved by caspase-8 with TNFα treatment, generating a GSDMC N-terminal domain that forms pores on the cell membrane and induces pyroptosis. Nuclear PD-L1, caspase-8 and GSDMC are required for macrophage-derived TNFα-induced tumour necrosis in vivo. Moreover, high expression of GSDMC correlates with poor survival. Antibiotic chemotherapy drugs induce pyroptosis in breast cancer. These findings identify a non-immune checkpoint function of PD-L1 and provide an unexpected concept that GSDMC/caspase-8 mediates a non-canonical pyroptosis pathway in cancer cells, causing tumour necrosis.
Although pyroptosis is critical for macrophages against pathogen infection, its role and mechanism in cancer cells remains unclear. PD-L1 has been detected in the nucleus, with unknown function. Here we show that PD-L1 switches TNFα-induced apoptosis to pyroptosis in cancer cells, resulting in tumour necrosis. Under hypoxia, p-Stat3 physically interacts with PD-L1 and facilitates its nuclear translocation, enhancing the transcription of the gasdermin C (GSDMC) gene. GSDMC is specifically cleaved by caspase-8 with TNFα treatment, generating a GSDMC N-terminal domain that forms pores on the cell membrane and induces pyroptosis. Nuclear PD-L1, caspase-8 and GSDMC are required for macrophage-derived TNFα-induced tumour necrosis in vivo. Moreover, high expression of GSDMC correlates with poor survival. Antibiotic chemotherapy drugs induce pyroptosis in breast cancer. These findings identify a non-immune checkpoint function of PD-L1 and provide an unexpected concept that GSDMC/caspase-8 mediates a non-canonical pyroptosis pathway in cancer cells, causing tumour necrosis.Hou et al. show that following hypoxia PD-L1 translocates into the nucleus to enhance transcription of GSDMC, which is then cleaved and activated by caspase-8 to cause pyroptosis in cancer cells.
Although pyroptosis is critical for macrophages against pathogen infection, its role and mechanism in cancer cells remains unclear. PD-L1 has been detected in the nucleus, with unknown function. Here we show that PD-L1 switches TNF[alpha]-induced apoptosis to pyroptosis in cancer cells, resulting in tumour necrosis. Under hypoxia, p-Stat3 physically interacts with PD-L1 and facilitates its nuclear translocation, enhancing the transcription of the gasdermin C (GSDMC) gene. GSDMC is specifically cleaved by caspase-8 with TNF[alpha] treatment, generating a GSDMC N-terminal domain that forms pores on the cell membrane and induces pyroptosis. Nuclear PD-L1, caspase-8 and GSDMC are required for macrophage-derived TNF[alpha]-induced tumour necrosis in vivo. Moreover, high expression of GSDMC correlates with poor survival. Antibiotic chemotherapy drugs induce pyroptosis in breast cancer. These findings identify a non-immune checkpoint function of PD-L1 and provide an unexpected concept that GSDMC/caspase-8 mediates a non-canonical pyroptosis pathway in cancer cells, causing tumour necrosis.
Although pyroptosis is critical for macrophages against pathogen infection, its role and mechanism in cancer cells remains unclear. PD-L1 has been detected in the nucleus, with unknown function. Here we show that PD-L1 switches TNFα-induced apoptosis to pyroptosis in cancer cells, resulting in tumour necrosis. Under hypoxia, p-Stat3 physically interacts with PD-L1 and facilitates its nuclear translocation, enhancing the transcription of the gasdermin C ( GSDMC ) gene. GSDMC is specifically cleaved by caspase-8 with TNFα treatment, generating a GSDMC N-terminal domain that forms pores on the cell membrane and induces pyroptosis. Nuclear PD-L1, caspase-8 and GSDMC are required for macrophage-derived TNFα-induced tumour necrosis in vivo. Moreover, high expression of GSDMC correlates with poor survival. Antibiotic chemotherapy drugs induce pyroptosis in breast cancer. These findings identify a non-immune checkpoint function of PD-L1 and provide an unexpected concept that GSDMC/caspase-8 mediates a non-canonical pyroptosis pathway in cancer cells, causing tumour necrosis. Hou et al. show that following hypoxia PD-L1 translocates into the nucleus to enhance transcription of GSDMC, which is then cleaved and activated by caspase-8 to cause pyroptosis in cancer cells.
Although pyroptosis is critical for macrophages against pathogen infection, its role and mechanism in cancer cells remains unclear. PD-L1 has been detected in the nucleus, with unknown function. Here we show that PD-L1 switches TNF[alpha]-induced apoptosis to pyroptosis in cancer cells, resulting in tumour necrosis. Under hypoxia, p-Stat3 physically interacts with PD-L1 and facilitates its nuclear translocation, enhancing the transcription of the gasdermin C (GSDMC) gene. GSDMC is specifically cleaved by caspase-8 with TNF[alpha] treatment, generating a GSDMC N-terminal domain that forms pores on the cell membrane and induces pyroptosis. Nuclear PD-L1, caspase-8 and GSDMC are required for macrophage-derived TNF[alpha]-induced tumour necrosis in vivo. Moreover, high expression of GSDMC correlates with poor survival. Antibiotic chemotherapy drugs induce pyroptosis in breast cancer. These findings identify a non-immune checkpoint function of PD-L1 and provide an unexpected concept that GSDMC/caspase-8 mediates a non-canonical pyroptosis pathway in cancer cells, causing tumour necrosis. Hou et al. show that following hypoxia PD-L1 translocates into the nucleus to enhance transcription of GSDMC, which is then cleaved and activated by caspase-8 to cause pyroptosis in cancer cells.
Audience Academic
Author You, Yun
Ke, Baozhen
Wu, Yun
Li, Yintao
Huang, Kebin
Hung, Mien-Chie
Chang, Chiung-Wen
Wang, Wei-Jan
Hou, Junwei
Nie, Lei
Hsu, Jung-Mao
Liu, Chunxiao
Chen, Yeh
Hsu, Jennifer L.
Li, Chia-Wei
Xia, Weiya
Ye, Zu
Tainer, John A.
Wang, Yu-Chuan
Shao, Bin
Zhao, Rongce
Yang, Yi
Xia, Xianghou
AuthorAffiliation 3 Department of Liver Surgery and Liver Transplantation Center, West China Hospital, Sichuan University, Chengdu 610041, China
7 State Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources, School of Chemistry and Pharmacy, Guangxi Normal University, Guilin 541004, China
4 Graduate Institute of Biomedical Sciences, Research Center for Cancer Biology, and Center for Molecular Medicine, China Medical University, Taichung 404, Taiwan
5 Department of Biotechnology, Asia University, Taichung 413, Taiwan
1 Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA
2 Department of Pathology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA
8 Key Laboratory of Carcinogenesis and Transformation Research (Ministry of Education), Department of Breast Oncology, Peking University Cancer Hospital and Institute, Beijing 100142, China
6 Institute of New Drug Development and Research Center for Cance
AuthorAffiliation_xml – name: 2 Department of Pathology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA
– name: 5 Department of Biotechnology, Asia University, Taichung 413, Taiwan
– name: 4 Graduate Institute of Biomedical Sciences, Research Center for Cancer Biology, and Center for Molecular Medicine, China Medical University, Taichung 404, Taiwan
– name: 3 Department of Liver Surgery and Liver Transplantation Center, West China Hospital, Sichuan University, Chengdu 610041, China
– name: 7 State Key Laboratory for Chemistry and Molecular Engineering of Medicinal Resources, School of Chemistry and Pharmacy, Guangxi Normal University, Guilin 541004, China
– name: 8 Key Laboratory of Carcinogenesis and Transformation Research (Ministry of Education), Department of Breast Oncology, Peking University Cancer Hospital and Institute, Beijing 100142, China
– name: 6 Institute of New Drug Development and Research Center for Cancer Biology, China Medical University, Taichung 404, Taiwan
– name: 9 Department of Biological Science and Technology, China Medical University, Taichung 404, Taiwan
– name: 1 Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA
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  givenname: Junwei
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  fullname: Zhao, Rongce
  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Department of Liver Surgery and Liver Transplantation Center, West China Hospital, Sichuan University, Department of Liver Surgery, Sun Yat-Sen University Cancer Center, State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine
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  givenname: Weiya
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  surname: Chang
  fullname: Chang, Chiung-Wen
  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center
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  givenname: Lei
  surname: Nie
  fullname: Nie, Lei
  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center
– sequence: 8
  givenname: Yeh
  surname: Chen
  fullname: Chen, Yeh
  organization: Graduate Institute of Biomedical Sciences, Research Center for Cancer Biology and Center for Molecular Medicine, China Medical University, Institute of New Drug Development, China Medical University
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  givenname: Yu-Chuan
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  organization: Graduate Institute of Biomedical Sciences, Research Center for Cancer Biology and Center for Molecular Medicine, China Medical University
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  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Department of Biological Science and Technology, China Medical University
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  givenname: Yun
  surname: Wu
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  organization: Department of Pathology, The University of Texas MD Anderson Cancer Center
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/32929201$$D View this record in MEDLINE/PubMed
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J.H. and M.-C.H. designed and conceived the study; J.H. and M.-C.H. wrote the manuscript; J.L.H. and K.H. contributed to the preparation of the manuscript. J.H., R.Z., W.X., Y.Y., J.-M.H., Y.C., Y.-C.W., C.L., W.-J.W., B.K., Z.Y., Y.Y., X.X., Y.L., C.-W.L., B.S., and J.A.T. performed experiments and analyzed data. L.N. and C.-W.C. analyzed PD-L1 and GSDMC sequences. Y.W. provided patient tissue samples. M.-C.H. supervised the entire project.
Author Contributions
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Snippet Although pyroptosis is critical for macrophages against pathogen infection, its role and mechanism in cancer cells remains unclear. PD-L1 has been detected in...
Pyroptosis is critical for macrophages against pathogen infection, but its role and mechanism in cancer cells remain unclear. PD-L1 has been detected in the...
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StartPage 1264
SubjectTerms 13/1
13/106
13/51
631/67
631/80/82
64/60
Animals
Antibiotics
Apoptosis
B7-H1 Antigen - genetics
B7-H1 Antigen - metabolism
Biomarkers, Tumor - genetics
Biomarkers, Tumor - metabolism
Biomedical and Life Sciences
Breast cancer
Cancer
Cancer cells
Cancer Research
Caspase-8
Cell Biology
Cell membranes
Cell Proliferation
Cellular proteins
Chemotherapy
Developmental Biology
DNA-Binding Proteins - genetics
DNA-Binding Proteins - metabolism
Female
Gene expression
Gene Expression Regulation, Neoplastic
Genetic aspects
Health aspects
Humans
Hypoxia
Hypoxia - physiopathology
Immune checkpoint
Immunosuppressive agents
Inflammasomes
Life Sciences
Macrophages
Mice
Mice, Inbred BALB C
Mice, Nude
Necrosis
Neoplasms - genetics
Neoplasms - metabolism
Neoplasms - pathology
Nuclear transport
Nuclei (cytology)
PD-L1 protein
Pyroptosis
Stat3 protein
Stem Cells
Switches
Transcription
Translocation
Tumor Cells, Cultured
Tumor necrosis factor-α
Tumor-Associated Macrophages
Tumors
Xenograft Model Antitumor Assays
Title PD-L1-mediated gasdermin C expression switches apoptosis to pyroptosis in cancer cells and facilitates tumour necrosis
URI https://link.springer.com/article/10.1038/s41556-020-0575-z
https://www.ncbi.nlm.nih.gov/pubmed/32929201
https://www.proquest.com/docview/2449455852
https://www.proquest.com/docview/2727100103
https://www.proquest.com/docview/2442848993
https://pubmed.ncbi.nlm.nih.gov/PMC7653546
Volume 22
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