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PMID: 25348003 Published · epublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Metastasis is regulated via microRNA-200/ZEB1 axis control of tumour cell PD-L1 expression and intratumoral immunosuppression.

Nature communications ·Vol. 5 ·2014-10-28 ·Pages 5241

Chen L, Gibbons DL, Goswami S, Cortez MA, Ahn YH, Byers LA, Zhang X, Yi X, Dwyer D, Lin W, Diao L, Wang J, Roybal J, Patel M, Ungewiss C, Peng D, Antonia S, Mediavilla-Varela M, Robertson G, Suraokar M, Welsh JW, Erez B, Wistuba II, Chen L, Peng D, Wang S, Ullrich SE, Heymach JV, Kurie JM, Qin FX

Abstract

Immunosuppression of tumour-infiltrating lymphocytes (TIL) is a common feature of advanced cancer, but its biological basis has remained obscure. We demonstrate here a molecular link between epithelial-to-mesenchymal transition (EMT) and CD8(+) TIL immunosuppression, two key drivers of cancer progression. We show that microRNA-200 (miR-200), a cell-autonomous suppressor of EMT and metastasis, targets PD-L1. Moreover, ZEB1, an EMT activator and transcriptional repressor of miR-200, relieves miR-200 repression of PD-L1 on tumour cells, leading to CD8(+) T-cell immunosuppression and metastasis. These findings are supported by robust correlations between the EMT score, miR-200 levels and PD-L1 expression in multiple human lung cancer datasets. In addition to revealing a link between EMT and T-cell dysfunction, these findings also show that ZEB1 promotes metastasis through a heretofore unappreciated cell non-autonomous mechanism, and suggest that subgroups of patients in whom malignant progression is driven by EMT activators may respond to treatment with PD-L1 antagonists.

MeSH Terms
Animals B7-H1 Antigen/metabolism CD8-Positive T-Lymphocytes Carcinoma, Non-Small-Cell Lung/genetics,immunology,pathology Cell Line, Tumor Cell Proliferation Databases as Topic Epithelial-Mesenchymal Transition/genetics Gene Targeting Homeodomain Proteins/metabolism Humans Immune Tolerance Immunity Kruppel-Like Transcription Factors/metabolism Lung Neoplasms/genetics,immunology,pathology Lymphocytes, Tumor-Infiltrating/immunology Male Mice, Inbred C57BL MicroRNAs/genetics,metabolism Models, Biological Neoplasm Metastasis Phenotype Transcription Factors/metabolism Zinc Finger E-box-Binding Homeobox 1
Chemicals
B7-H1 Antigen CD274 protein, human Cd274 protein, mouse Homeodomain Proteins Kruppel-Like Transcription Factors MIRN200 microRNA, human MicroRNAs Mirn200 microRNA, mouse Transcription Factors ZEB1 protein, human ZEB1 protein, mouse Zinc Finger E-box-Binding Homeobox 1
Authors & Affiliations
30 authors, click to expand affiliations / ORCID
Chen Limo
Department of Thoracic/Head and Neck Medical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA. | Department of Immunology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
Gibbons Don L
Department of Thoracic/Head and Neck Medical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA. | Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
Goswami Sangeeta
Department of Thoracic/Head and Neck Medical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
Cortez Maria Angelica
Department of Thoracic/Head and Neck Medical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
Ahn Young-Ho
Department of Thoracic/Head and Neck Medical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA. | Department of Molecular Medicine, Ewha Womans University School of Medicine, 1071 Anyangcheonro, Yangcheon-gu, Seoul 158-710, Korea.
Byers Lauren A
Department of Thoracic/Head and Neck Medical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
Zhang Xuejun
Department of Immunology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
Yi Xiaohui
Department of Immunology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
Dwyer David
Department of Immunology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
Lin Wei
Department of Thoracic/Head and Neck Medical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
Diao Lixia
Department of Bioinformatics & Computational Biology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
Wang Jing
Department of Bioinformatics & Computational Biology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
Roybal Jonathon
Department of Thoracic/Head and Neck Medical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
Patel Mayuri
Department of Thoracic/Head and Neck Medical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
Ungewiss Christin
Department of Thoracic/Head and Neck Medical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
Peng David
Department of Thoracic/Head and Neck Medical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
Antonia Scott
Department of Immunology, H. Lee Moffitt Cancer Center, Tampa, FL33612, USA.
Mediavilla-Varela Melanie
Department of Immunology, H. Lee Moffitt Cancer Center, Tampa, FL33612, USA.
Robertson Gordon
Canada's Michael Smith Genome Sciences Centre, BC Cancer Agency, Vancouver, British Columbia V5Z, Canada.
Suraokar Milind
Department of Thoracic/Head and Neck Medical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA. | Department of Translational and Molecular Pathology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
Welsh James W
Department of Experimental Radiation Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
Erez Baruch
Department of Thoracic/Head and Neck Medical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
Wistuba Ignacio I
Department of Thoracic/Head and Neck Medical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA. | Department of Translational and Molecular Pathology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
Chen Lieping
Department of Immunobiology, Yale School of Medicine, 10 Amistad Street, New Haven, CT 06519, USA.
Peng Di
Key Laboratory of Gene Engineering of the Ministry of Education and State Key Laboratory for Biocontrol, Sun Yat-Sen University, Guangzhou, 510275, China.
Wang Shanshan
Key Laboratory of Gene Engineering of the Ministry of Education and State Key Laboratory for Biocontrol, Sun Yat-Sen University, Guangzhou, 510275, China.
Ullrich Stephen E
Department of Immunology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
Heymach John V
Department of Thoracic/Head and Neck Medical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
Kurie Jonathan M
Department of Thoracic/Head and Neck Medical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
Qin F Xiao-Feng
Department of Thoracic/Head and Neck Medical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA. | Department of Immunology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA. | Key Laboratory of Gene Engineering of the Ministry of Education and State Key Laboratory for Biocontrol, Sun Yat-Sen University, Guangzhou, 510275, China.
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Article Info
Journal
Nature communications
Abbr.
Nat Commun
ISSN
2041-1723
Published
2014-10-28
Epub
2014-00-28
Pages
5241
Language
English
Region
England
NLM ID
101528555
PMCID
PMC4212319
Subset
IM
Grants
NCI NIH HHS · P30 CA016672 · United States
NCI NIH HHS · T32 CA009299-32 · United States
NCI NIH HHS · 5-R01-CA168484-04 · United States
NCI NIH HHS · 5-R01-CA132608-03 · United States
NCI NIH HHS · R01 CA168484 · United States
NCI NIH HHS · P30CA016672 · United States
NCI NIH HHS · 5-P50-CA70907-12 PP-3B · United States
NCI NIH HHS · CA016672 · United States
NCI NIH HHS · P30 CA076292 · United States
NCI NIH HHS · R01 CA132608 · United States
NCI NIH HHS · P50 CA070907 · United States
NCI NIH HHS · K08 CA151651 · United States
NCI NIH HHS · T32 CA009299 · United States
NCI NIH HHS · 5-P50-CA70907-12 PP-3 · United States
NCI NIH HHS · K08-CA151651 · United States
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