MET Inhibitors Promote Liver Tumor Evasion of the Immune Response by Stabilizing PDL1

Inhibitors of MET have not produced satisfactory outcomes in trials of patients with liver cancer. We investigated the mechanisms of liver tumor resistance to MET inhibitors in mice. We tested the effects of MET inhibitors tivantinib and capmatinib in the mouse hepatocellular carcinoma (HCC) cell li...

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Vydané v:Gastroenterology (New York, N.Y. 1943) Ročník 156; číslo 6; s. 1849
Hlavní autori: Li, Hui, Li, Chia-Wei, Li, Xiaoqiang, Ding, Qingqing, Guo, Lei, Liu, Shuang, Liu, Chunxiao, Lai, Chien-Chen, Hsu, Jung-Mao, Dong, Qiongzhu, Xia, Weiya, Hsu, Jennifer L, Yamaguchi, Hirohito, Du, Yi, Lai, Yun-Ju, Sun, Xian, Koller, Paul B, Ye, Qinghai, Hung, Mien-Chie
Médium: Journal Article
Jazyk:English
Vydavateľské údaje: United States 01.05.2019
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ISSN:1528-0012, 1528-0012
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Abstract Inhibitors of MET have not produced satisfactory outcomes in trials of patients with liver cancer. We investigated the mechanisms of liver tumor resistance to MET inhibitors in mice. We tested the effects of MET inhibitors tivantinib and capmatinib in the mouse hepatocellular carcinoma (HCC) cell line HCA-1 and in immune-competent and immunodeficient mice with subcutaneous tumors grown from this cell line. Tumors were collected from mice and tumor cells were analyzed by time-of-flight mass cytometry. We used short hairpin RNAs to weaken expression of MET in Hep3B, SK-HEP-1, HA59T, and HA22T liver cancer cell lines and analyzed cells by immunoblot, immunofluorescence, and immunoprecipitation assays. Mass spectrometry was used to assess interactions between MET and glycogen synthase kinase 3β (GSK3B), and GSK3B phosphorylation, in liver cancer cell lines. C57/BL6 mice with orthotopic tumors grown from Hep1-6 cells were given combinations of capmatinib or tivantinib and antibodies against programmed cell death 1 (PDCD1; also called PD1); tumors were collected and analyzed by immunofluorescence. We analyzed 268 HCCsamples in a tissue microarray by immunohistochemistry. Exposure of liver cancer cell lines to MET inhibitors increased their expression of PD ligand 1 (PDL1) and inactivated cocultured T cells. MET phosphorylated and activated GSK3B at tyrosine 56, which decreased the expression of PDL1 by liver cancer cells. In orthotopic tumors grown in immune-competent mice, MET inhibitors decreased the antitumor activity of T cells. However, addition of anti-PD1 decreased orthotopic tumor growth and prolonged survival of mice compared with anti-PD1 or MET inhibitors alone. Tissue microarray analysis of HCC samples showed an inverse correlation between levels of MET and PDL1 and a positive correlation between levels of MET and phosphorylated GSK3B. In studies of liver cancer cell lines and mice with orthotopic tumors, MET mediated phosphorylation and activated GSK3B, leading to decreased expression of PDL1. Combined with a MET inhibitor, anti-PD1 and anti-PDL1 produced additive effect to slow growth of HCCs in mice.
AbstractList Inhibitors of MET have not produced satisfactory outcomes in trials of patients with liver cancer. We investigated the mechanisms of liver tumor resistance to MET inhibitors in mice.BACKGROUND & AIMSInhibitors of MET have not produced satisfactory outcomes in trials of patients with liver cancer. We investigated the mechanisms of liver tumor resistance to MET inhibitors in mice.We tested the effects of MET inhibitors tivantinib and capmatinib in the mouse hepatocellular carcinoma (HCC) cell line HCA-1 and in immune-competent and immunodeficient mice with subcutaneous tumors grown from this cell line. Tumors were collected from mice and tumor cells were analyzed by time-of-flight mass cytometry. We used short hairpin RNAs to weaken expression of MET in Hep3B, SK-HEP-1, HA59T, and HA22T liver cancer cell lines and analyzed cells by immunoblot, immunofluorescence, and immunoprecipitation assays. Mass spectrometry was used to assess interactions between MET and glycogen synthase kinase 3β (GSK3B), and GSK3B phosphorylation, in liver cancer cell lines. C57/BL6 mice with orthotopic tumors grown from Hep1-6 cells were given combinations of capmatinib or tivantinib and antibodies against programmed cell death 1 (PDCD1; also called PD1); tumors were collected and analyzed by immunofluorescence. We analyzed 268 HCCsamples in a tissue microarray by immunohistochemistry.METHODSWe tested the effects of MET inhibitors tivantinib and capmatinib in the mouse hepatocellular carcinoma (HCC) cell line HCA-1 and in immune-competent and immunodeficient mice with subcutaneous tumors grown from this cell line. Tumors were collected from mice and tumor cells were analyzed by time-of-flight mass cytometry. We used short hairpin RNAs to weaken expression of MET in Hep3B, SK-HEP-1, HA59T, and HA22T liver cancer cell lines and analyzed cells by immunoblot, immunofluorescence, and immunoprecipitation assays. Mass spectrometry was used to assess interactions between MET and glycogen synthase kinase 3β (GSK3B), and GSK3B phosphorylation, in liver cancer cell lines. C57/BL6 mice with orthotopic tumors grown from Hep1-6 cells were given combinations of capmatinib or tivantinib and antibodies against programmed cell death 1 (PDCD1; also called PD1); tumors were collected and analyzed by immunofluorescence. We analyzed 268 HCCsamples in a tissue microarray by immunohistochemistry.Exposure of liver cancer cell lines to MET inhibitors increased their expression of PD ligand 1 (PDL1) and inactivated cocultured T cells. MET phosphorylated and activated GSK3B at tyrosine 56, which decreased the expression of PDL1 by liver cancer cells. In orthotopic tumors grown in immune-competent mice, MET inhibitors decreased the antitumor activity of T cells. However, addition of anti-PD1 decreased orthotopic tumor growth and prolonged survival of mice compared with anti-PD1 or MET inhibitors alone. Tissue microarray analysis of HCC samples showed an inverse correlation between levels of MET and PDL1 and a positive correlation between levels of MET and phosphorylated GSK3B.RESULTSExposure of liver cancer cell lines to MET inhibitors increased their expression of PD ligand 1 (PDL1) and inactivated cocultured T cells. MET phosphorylated and activated GSK3B at tyrosine 56, which decreased the expression of PDL1 by liver cancer cells. In orthotopic tumors grown in immune-competent mice, MET inhibitors decreased the antitumor activity of T cells. However, addition of anti-PD1 decreased orthotopic tumor growth and prolonged survival of mice compared with anti-PD1 or MET inhibitors alone. Tissue microarray analysis of HCC samples showed an inverse correlation between levels of MET and PDL1 and a positive correlation between levels of MET and phosphorylated GSK3B.In studies of liver cancer cell lines and mice with orthotopic tumors, MET mediated phosphorylation and activated GSK3B, leading to decreased expression of PDL1. Combined with a MET inhibitor, anti-PD1 and anti-PDL1 produced additive effect to slow growth of HCCs in mice.CONCLUSIONSIn studies of liver cancer cell lines and mice with orthotopic tumors, MET mediated phosphorylation and activated GSK3B, leading to decreased expression of PDL1. Combined with a MET inhibitor, anti-PD1 and anti-PDL1 produced additive effect to slow growth of HCCs in mice.
Inhibitors of MET have not produced satisfactory outcomes in trials of patients with liver cancer. We investigated the mechanisms of liver tumor resistance to MET inhibitors in mice. We tested the effects of MET inhibitors tivantinib and capmatinib in the mouse hepatocellular carcinoma (HCC) cell line HCA-1 and in immune-competent and immunodeficient mice with subcutaneous tumors grown from this cell line. Tumors were collected from mice and tumor cells were analyzed by time-of-flight mass cytometry. We used short hairpin RNAs to weaken expression of MET in Hep3B, SK-HEP-1, HA59T, and HA22T liver cancer cell lines and analyzed cells by immunoblot, immunofluorescence, and immunoprecipitation assays. Mass spectrometry was used to assess interactions between MET and glycogen synthase kinase 3β (GSK3B), and GSK3B phosphorylation, in liver cancer cell lines. C57/BL6 mice with orthotopic tumors grown from Hep1-6 cells were given combinations of capmatinib or tivantinib and antibodies against programmed cell death 1 (PDCD1; also called PD1); tumors were collected and analyzed by immunofluorescence. We analyzed 268 HCCsamples in a tissue microarray by immunohistochemistry. Exposure of liver cancer cell lines to MET inhibitors increased their expression of PD ligand 1 (PDL1) and inactivated cocultured T cells. MET phosphorylated and activated GSK3B at tyrosine 56, which decreased the expression of PDL1 by liver cancer cells. In orthotopic tumors grown in immune-competent mice, MET inhibitors decreased the antitumor activity of T cells. However, addition of anti-PD1 decreased orthotopic tumor growth and prolonged survival of mice compared with anti-PD1 or MET inhibitors alone. Tissue microarray analysis of HCC samples showed an inverse correlation between levels of MET and PDL1 and a positive correlation between levels of MET and phosphorylated GSK3B. In studies of liver cancer cell lines and mice with orthotopic tumors, MET mediated phosphorylation and activated GSK3B, leading to decreased expression of PDL1. Combined with a MET inhibitor, anti-PD1 and anti-PDL1 produced additive effect to slow growth of HCCs in mice.
Author Yamaguchi, Hirohito
Li, Xiaoqiang
Ding, Qingqing
Hung, Mien-Chie
Lai, Yun-Ju
Li, Hui
Guo, Lei
Liu, Chunxiao
Hsu, Jung-Mao
Li, Chia-Wei
Hsu, Jennifer L
Xia, Weiya
Sun, Xian
Ye, Qinghai
Lai, Chien-Chen
Koller, Paul B
Dong, Qiongzhu
Du, Yi
Liu, Shuang
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  givenname: Hui
  surname: Li
  fullname: Li, Hui
  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas; Department of Liver Surgery and Transplantation, Liver Cancer Institute, Zhongshan Hospital, Fudan University and Key Laboratory of Carcinogenesis and Cancer Invasion, Ministry of Education, Shanghai, People's Republic of China
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  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas
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  givenname: Xiaoqiang
  surname: Li
  fullname: Li, Xiaoqiang
  organization: Department of Thoracic Surgery, Peking University Shenzhen Hospital, Shenzhen, People's Republic of China
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  givenname: Qingqing
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  fullname: Ding, Qingqing
  organization: Department of Pathology, University of Kansas Medical Center, Kansas City, Kansas
– sequence: 5
  givenname: Lei
  surname: Guo
  fullname: Guo, Lei
  organization: Department of Liver Surgery and Transplantation, Liver Cancer Institute, Zhongshan Hospital, Fudan University and Key Laboratory of Carcinogenesis and Cancer Invasion, Ministry of Education, Shanghai, People's Republic of China
– sequence: 6
  givenname: Shuang
  surname: Liu
  fullname: Liu, Shuang
  organization: Department of Liver Surgery and Transplantation, Liver Cancer Institute, Zhongshan Hospital, Fudan University and Key Laboratory of Carcinogenesis and Cancer Invasion, Ministry of Education, Shanghai, People's Republic of China
– sequence: 7
  givenname: Chunxiao
  surname: Liu
  fullname: Liu, Chunxiao
  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas
– sequence: 8
  givenname: Chien-Chen
  surname: Lai
  fullname: Lai, Chien-Chen
  organization: Graduate Institute of Biomedical Sciences and Center for Molecular Medicine, China Medical University, Taichung, Taiwan; Institute of Molecular Biology, National Chung Hsing University, Taichung, Taiwan
– sequence: 9
  givenname: Jung-Mao
  surname: Hsu
  fullname: Hsu, Jung-Mao
  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas
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  givenname: Qiongzhu
  surname: Dong
  fullname: Dong, Qiongzhu
  organization: Institutes of Biomedical Sciences, Fudan University, Shanghai, People's Republic of China
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  givenname: Weiya
  surname: Xia
  fullname: Xia, Weiya
  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas
– sequence: 12
  givenname: Jennifer L
  surname: Hsu
  fullname: Hsu, Jennifer L
  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas; Graduate Institute of Biomedical Sciences and Center for Molecular Medicine, China Medical University, Taichung, Taiwan
– sequence: 13
  givenname: Hirohito
  surname: Yamaguchi
  fullname: Yamaguchi, Hirohito
  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas
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  givenname: Yi
  surname: Du
  fullname: Du, Yi
  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas
– sequence: 15
  givenname: Yun-Ju
  surname: Lai
  fullname: Lai, Yun-Ju
  organization: Department of Neurology, McGovern Medical School, The University of Texas Health Science Center at Houston, Houston, Texas
– sequence: 16
  givenname: Xian
  surname: Sun
  fullname: Sun, Xian
  organization: Department of Medical Oncology, Harbin Medical University Cancer Hospital, Harbin, People's Republic of China
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  givenname: Paul B
  surname: Koller
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  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas
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  givenname: Qinghai
  surname: Ye
  fullname: Ye, Qinghai
  organization: Department of Liver Surgery and Transplantation, Liver Cancer Institute, Zhongshan Hospital, Fudan University and Key Laboratory of Carcinogenesis and Cancer Invasion, Ministry of Education, Shanghai, People's Republic of China
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  givenname: Mien-Chie
  surname: Hung
  fullname: Hung, Mien-Chie
  email: mhung@mdanderson.org
  organization: Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas; Graduate Institute of Biomedical Sciences and Center for Molecular Medicine, China Medical University, Taichung, Taiwan. Electronic address: mhung@mdanderson.org
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ContentType Journal Article
Copyright Copyright © 2019 AGA Institute. Published by Elsevier Inc. All rights reserved.
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Issue 6
Keywords Glycogen Synthase Kinase 3
Programmed Cell Death Ligand 1
Hepatocellular Carcinoma
Tumor Necrosis Factor Receptor-Associated Factor 6
Language English
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OpenAccessLink https://www.ncbi.nlm.nih.gov/pmc/articles/6904924
PMID 30711629
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PublicationDate 2019-05-01
PublicationDateYYYYMMDD 2019-05-01
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  year: 2019
  text: 2019-05-01
  day: 01
PublicationDecade 2010
PublicationPlace United States
PublicationPlace_xml – name: United States
PublicationTitle Gastroenterology (New York, N.Y. 1943)
PublicationTitleAlternate Gastroenterology
PublicationYear 2019
References 30926349 - Gastroenterology. 2019 May;156(6):1563-1565
References_xml – reference: 30926349 - Gastroenterology. 2019 May;156(6):1563-1565
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Snippet Inhibitors of MET have not produced satisfactory outcomes in trials of patients with liver cancer. We investigated the mechanisms of liver tumor resistance to...
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SubjectTerms Animals
Antibodies, Monoclonal - therapeutic use
Antineoplastic Agents - pharmacology
Antineoplastic Agents - therapeutic use
B7-H1 Antigen - antagonists & inhibitors
B7-H1 Antigen - immunology
B7-H1 Antigen - metabolism
Carcinoma, Hepatocellular - drug therapy
Carcinoma, Hepatocellular - enzymology
Carcinoma, Hepatocellular - immunology
Cell Line, Tumor
Down-Regulation
Glycogen Synthase Kinase 3 beta - metabolism
Granzymes - metabolism
Imidazoles - pharmacology
Imidazoles - therapeutic use
Liver Neoplasms - drug therapy
Liver Neoplasms - enzymology
Liver Neoplasms - immunology
Male
Mice
Phosphorylation
Proto-Oncogene Proteins c-met - antagonists & inhibitors
Proto-Oncogene Proteins c-met - metabolism
Pyrrolidinones - pharmacology
Pyrrolidinones - therapeutic use
Quinolines - pharmacology
Quinolines - therapeutic use
TNF Receptor-Associated Factor 6 - immunology
TNF Receptor-Associated Factor 6 - metabolism
Triazines - pharmacology
Triazines - therapeutic use
Tumor Escape - drug effects
Ubiquitination
Title MET Inhibitors Promote Liver Tumor Evasion of the Immune Response by Stabilizing PDL1
URI https://www.ncbi.nlm.nih.gov/pubmed/30711629
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Volume 156
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