Single tumor-initiating cells evade immune clearance by recruiting type II macrophages

Tumor infiltrated type II (M2) macrophages promote tumorigenesis by suppressing immune clearance, promoting proliferation, and stimulating angiogenesis. Interestingly, macrophages were also found to enrich in small foci of altered hepatocytes containing liver tumor-initiating cells (TICs). However,...

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Published inGenes & development Vol. 31; no. 3; pp. 247 - 259
Main Authors Guo, Xiaocan, Zhao, Yang, Yan, Huan, Yang, Yingcheng, Shen, Shuying, Dai, Xiaoming, Ji, Xinyan, Ji, Fubo, Gong, Xing-Guo, Li, Li, Bai, Xueli, Feng, Xin-Hua, Liang, Tingbo, Ji, Junfang, Chen, Lei, Wang, Hongyang, Zhao, Bin
Format Journal Article
LanguageEnglish
Published United States Cold Spring Harbor Laboratory Press 01.02.2017
Subjects
Adaptor Proteins, Signal Transducing - genetics
Adaptor Proteins, Signal Transducing - metabolism
Animals
Carcinoma, Hepatocellular - immunology
Carcinoma, Hepatocellular - metabolism
Carcinoma, Hepatocellular - pathology
Cell Communication - immunology
Cell Cycle Proteins
Cell Transformation, Neoplastic - immunology
Cell Transformation, Neoplastic - metabolism
Cell Transformation, Neoplastic - pathology
Cells, Cultured
Hepatocyte Growth Factor - physiology
Hepatocytes - immunology
Hepatocytes - metabolism
Hepatocytes - pathology
Homeodomain Proteins - physiology
Humans
Liver Neoplasms - immunology
Liver Neoplasms - metabolism
Liver Neoplasms - pathology
Macrophages - cytology
Macrophages - immunology
Male
Mice
Mice, Inbred ICR
Mice, Knockout
Neoplastic Stem Cells - cytology
Neoplastic Stem Cells - immunology
Phosphoproteins - genetics
Phosphoproteins - metabolism
Protein-Serine-Threonine Kinases - physiology
Proto-Oncogene Proteins - physiology
Research Paper
Tumor Suppressor Protein p53 - physiology
YAP
macrophage
liver cancer
tumor-initiating cell
Hippo pathway
immunosurveillance
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Abstract Tumor infiltrated type II (M2) macrophages promote tumorigenesis by suppressing immune clearance, promoting proliferation, and stimulating angiogenesis. Interestingly, macrophages were also found to enrich in small foci of altered hepatocytes containing liver tumor-initiating cells (TICs). However, whether and how TICs specifically recruit macrophages and the function of these macrophages in tumor initiation remain unknown due to technical difficulties. In this study, by generating genetically defined liver TICs, we demonstrate that TICs actively recruit M2 macrophages from as early as the single-cell stage. Elimination of TIC-associated macrophages (TICAMs) abolishes tumorigenesis in a manner dependent on the immune system. Mechanistically, activation of the Hippo pathway effector Yes-associated protein (YAP) underlies macrophage recruitment by TICs. These results demonstrate for the first time that macrophages play a decisive role in the survival of single TICs in vivo and provide a proof of principle for TIC elimination by targeting YAP or M2 macrophages.
AbstractList Tumor infiltrated type II (M2) macrophages promote tumorigenesis by suppressing immune clearance, promoting proliferation, and stimulating angiogenesis. Interestingly, macrophages were also found to enrich in small foci of altered hepatocytes containing liver tumor-initiating cells (TICs). However, whether and how TICs specifically recruit macrophages and the function of these macrophages in tumor initiation remain unknown due to technical difficulties. In this study, by generating genetically defined liver TICs, we demonstrate that TICs actively recruit M2 macrophages from as early as the single-cell stage. Elimination of TIC-associated macrophages (TICAMs) abolishes tumorigenesis in a manner dependent on the immune system. Mechanistically, activation of the Hippo pathway effector Yes-associated protein (YAP) underlies macrophage recruitment by TICs. These results demonstrate for the first time that macrophages play a decisive role in the survival of single TICs in vivo and provide a proof of principle for TIC elimination by targeting YAP or M2 macrophages.
Guo et al. show that liver tumor-initiating cells (TICs) actively recruit M2 macrophages from as early as the single-cell stage. Elimination of TIC-associated macrophages abolishes tumorigenesis in a manner dependent on the immune system. Tumor infiltrated type II (M2) macrophages promote tumorigenesis by suppressing immune clearance, promoting proliferation, and stimulating angiogenesis. Interestingly, macrophages were also found to enrich in small foci of altered hepatocytes containing liver tumor-initiating cells (TICs). However, whether and how TICs specifically recruit macrophages and the function of these macrophages in tumor initiation remain unknown due to technical difficulties. In this study, by generating genetically defined liver TICs, we demonstrate that TICs actively recruit M2 macrophages from as early as the single-cell stage. Elimination of TIC-associated macrophages (TICAMs) abolishes tumorigenesis in a manner dependent on the immune system. Mechanistically, activation of the Hippo pathway effector Yes-associated protein (YAP) underlies macrophage recruitment by TICs. These results demonstrate for the first time that macrophages play a decisive role in the survival of single TICs in vivo and provide a proof of principle for TIC elimination by targeting YAP or M2 macrophages.
Author Feng, Xin-Hua
Li, Li
Liang, Tingbo
Chen, Lei
Shen, Shuying
Yan, Huan
Ji, Fubo
Ji, Xinyan
Ji, Junfang
Bai, Xueli
Yang, Yingcheng
Wang, Hongyang
Zhao, Yang
Dai, Xiaoming
Gong, Xing-Guo
Guo, Xiaocan
Zhao, Bin
AuthorAffiliation 3 Institute of Biochemistry, College of Life Science, Zhejiang University, Hangzhou, Zhejiang 310058, China
4 Institute of Aging Research, Hangzhou Normal University, Hangzhou, Zhejiang 311121, China
2 International Co-operation Laboratory on Signal Transduction, Eastern Hepatobiliary Surgery Institute, Second Military Medical University, Shanghai 200438, China
5 Department of Hepatobiliary and Pancreatic Surgery, Key Laboratory of Cancer Prevention and Intervention, The Second Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang 310058, China
1 Life Sciences Institute, Innovation Center for Cell Signaling Network, Zhejiang University, Hangzhou, Zhejiang 310058, China
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– name: 4 Institute of Aging Research, Hangzhou Normal University, Hangzhou, Zhejiang 311121, China
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– name: 1 Life Sciences Institute, Innovation Center for Cell Signaling Network, Zhejiang University, Hangzhou, Zhejiang 310058, China
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  organization: Life Sciences Institute, Innovation Center for Cell Signaling Network, Zhejiang University, Hangzhou, Zhejiang 310058, China
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Issue 3
Keywords YAP
macrophage
liver cancer
tumor-initiating cell
Hippo pathway
immunosurveillance
Language English
License 2017 Guo et al.; Published by Cold Spring Harbor Laboratory Press.
This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genesdev.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
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Snippet Tumor infiltrated type II (M2) macrophages promote tumorigenesis by suppressing immune clearance, promoting proliferation, and stimulating angiogenesis....
Guo et al. show that liver tumor-initiating cells (TICs) actively recruit M2 macrophages from as early as the single-cell stage. Elimination of TIC-associated...
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SubjectTerms Adaptor Proteins, Signal Transducing - genetics
Adaptor Proteins, Signal Transducing - metabolism
Animals
Carcinoma, Hepatocellular - immunology
Carcinoma, Hepatocellular - metabolism
Carcinoma, Hepatocellular - pathology
Cell Communication - immunology
Cell Cycle Proteins
Cell Transformation, Neoplastic - immunology
Cell Transformation, Neoplastic - metabolism
Cell Transformation, Neoplastic - pathology
Cells, Cultured
Hepatocyte Growth Factor - physiology
Hepatocytes - immunology
Hepatocytes - metabolism
Hepatocytes - pathology
Homeodomain Proteins - physiology
Humans
Liver Neoplasms - immunology
Liver Neoplasms - metabolism
Liver Neoplasms - pathology
Macrophages - cytology
Macrophages - immunology
Male
Mice
Mice, Inbred ICR
Mice, Knockout
Neoplastic Stem Cells - cytology
Neoplastic Stem Cells - immunology
Phosphoproteins - genetics
Phosphoproteins - metabolism
Protein-Serine-Threonine Kinases - physiology
Proto-Oncogene Proteins - physiology
Research Paper
Tumor Suppressor Protein p53 - physiology
Title Single tumor-initiating cells evade immune clearance by recruiting type II macrophages
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