Vascular niche IL-6 induces alternative macrophage activation in glioblastoma through HIF-2α

Spatiotemporal regulation of tumor immunity remains largely unexplored. Here we identify a vascular niche that controls alternative macrophage activation in glioblastoma (GBM). We show that tumor-promoting macrophages are spatially proximate to GBM-associated endothelial cells (ECs), permissive for...

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Published inNature communications Vol. 9; no. 1; pp. 559 - 15
Main Authors Wang, Qirui, He, Zhenqiang, Huang, Menggui, Liu, Tianrun, Wang, Yanling, Xu, Haineng, Duan, Hao, Ma, Peihong, Zhang, Lin, Zamvil, Scott S., Hidalgo, Juan, Zhang, Zhenfeng, O’Rourke, Donald M., Dahmane, Nadia, Brem, Steven, Mou, Yonggao, Gong, Yanqing, Fan, Yi
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 08.02.2018
Nature Publishing Group
Nature Portfolio
Subjects
13/31
14/5
45/77
45/88
45/90
631/67/1922
631/67/327
64/110
96/1
Animals
Arginase
Arginase - immunology
Basic Helix-Loop-Helix Transcription Factors - genetics
Brain cancer
Cancer
Cancer therapies
Cell activation
Cell Line, Tumor
Cells, Cultured
Colony-stimulating factor
Cytokines
Disease Progression
Endothelial cells
Endothelial Cells - immunology
Flow cytometry
Glioblastoma
Glioblastoma - immunology
Growth factors
Human subjects
Humanities and Social Sciences
Humans
Hypoxia
Hypoxia-inducible factors
Immunity
Immunology
Interleukin 6
Interleukin-6 - immunology
Macrophage Activation - immunology
Macrophage colony-stimulating factor
Macrophage Colony-Stimulating Factor - immunology
Macrophages
Macrophages - immunology
Medicine
Mice
Microvessels - cytology
Monocytes - immunology
multidisciplinary
Neoplasms, Experimental - immunology
Neurosurgery
Nitric oxide
Otolaryngology
Peroxisome proliferator-activated receptors
Polarization
Polyamines
Radiation
Rodents
Science
Science (multidisciplinary)
Survival
Transcription activation
Transcriptional Activation
Tumor Microenvironment
Tumors
Online AccessGet full text

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Abstract Spatiotemporal regulation of tumor immunity remains largely unexplored. Here we identify a vascular niche that controls alternative macrophage activation in glioblastoma (GBM). We show that tumor-promoting macrophages are spatially proximate to GBM-associated endothelial cells (ECs), permissive for angiocrine-induced macrophage polarization. We identify ECs as one of the major sources for interleukin-6 (IL-6) expression in GBM microenvironment. Furthermore, we reveal that colony-stimulating factor-1 and angiocrine IL-6 induce robust arginase-1 expression and macrophage alternative activation, mediated through peroxisome proliferator-activated receptor-γ-dependent transcriptional activation of hypoxia-inducible factor-2α. Finally, utilizing a genetic murine GBM model, we show that EC-specific knockout of IL-6 inhibits macrophage alternative activation and improves survival in the GBM-bearing mice. These findings illustrate a vascular niche-dependent mechanism for alternative macrophage activation and cancer progression, and suggest that targeting endothelial IL-6 may offer a selective and efficient therapeutic strategy for GBM, and possibly other solid malignant tumors. Macrophages in the tumour microenvironment (TME) acquire tumour-promoting functions upon M2 polarization. Here the authors show, in a mouse model of glioblastoma, that endothelial cells in the TME induce macrophage M2 polarization via IL-6 and that depletion of endothelial IL-6 improves survival.
AbstractList Spatiotemporal regulation of tumor immunity remains largely unexplored. Here we identify a vascular niche that controls alternative macrophage activation in glioblastoma (GBM). We show that tumor-promoting macrophages are spatially proximate to GBM-associated endothelial cells (ECs), permissive for angiocrine-induced macrophage polarization. We identify ECs as one of the major sources for interleukin-6 (IL-6) expression in GBM microenvironment. Furthermore, we reveal that colony-stimulating factor-1 and angiocrine IL-6 induce robust arginase-1 expression and macrophage alternative activation, mediated through peroxisome proliferator-activated receptor-γ-dependent transcriptional activation of hypoxia-inducible factor-2α. Finally, utilizing a genetic murine GBM model, we show that EC-specific knockout of IL-6 inhibits macrophage alternative activation and improves survival in the GBM-bearing mice. These findings illustrate a vascular niche-dependent mechanism for alternative macrophage activation and cancer progression, and suggest that targeting endothelial IL-6 may offer a selective and efficient therapeutic strategy for GBM, and possibly other solid malignant tumors.
Spatiotemporal regulation of tumor immunity remains largely unexplored. Here we identify a vascular niche that controls alternative macrophage activation in glioblastoma (GBM). We show that tumor-promoting macrophages are spatially proximate to GBM-associated endothelial cells (ECs), permissive for angiocrine-induced macrophage polarization. We identify ECs as one of the major sources for interleukin-6 (IL-6) expression in GBM microenvironment. Furthermore, we reveal that colony-stimulating factor-1 and angiocrine IL-6 induce robust arginase-1 expression and macrophage alternative activation, mediated through peroxisome proliferator-activated receptor-γ-dependent transcriptional activation of hypoxia-inducible factor-2α. Finally, utilizing a genetic murine GBM model, we show that EC-specific knockout of IL-6 inhibits macrophage alternative activation and improves survival in the GBM-bearing mice. These findings illustrate a vascular niche-dependent mechanism for alternative macrophage activation and cancer progression, and suggest that targeting endothelial IL-6 may offer a selective and efficient therapeutic strategy for GBM, and possibly other solid malignant tumors. Macrophages in the tumour microenvironment (TME) acquire tumour-promoting functions upon M2 polarization. Here the authors show, in a mouse model of glioblastoma, that endothelial cells in the TME induce macrophage M2 polarization via IL-6 and that depletion of endothelial IL-6 improves survival.
Spatiotemporal regulation of tumor immunity remains largely unexplored. Here we identify a vascular niche that controls alternative macrophage activation in glioblastoma (GBM). We show that tumor-promoting macrophages are spatially proximate to GBM-associated endothelial cells (ECs), permissive for angiocrine-induced macrophage polarization. We identify ECs as one of the major sources for interleukin-6 (IL-6) expression in GBM microenvironment. Furthermore, we reveal that colony-stimulating factor-1 and angiocrine IL-6 induce robust arginase-1 expression and macrophage alternative activation, mediated through peroxisome proliferator-activated receptor-γ-dependent transcriptional activation of hypoxia-inducible factor-2α. Finally, utilizing a genetic murine GBM model, we show that EC-specific knockout of IL-6 inhibits macrophage alternative activation and improves survival in the GBM-bearing mice. These findings illustrate a vascular niche-dependent mechanism for alternative macrophage activation and cancer progression, and suggest that targeting endothelial IL-6 may offer a selective and efficient therapeutic strategy for GBM, and possibly other solid malignant tumors.Macrophages in the tumour microenvironment (TME) acquire tumour-promoting functions upon M2 polarization. Here the authors show, in a mouse model of glioblastoma, that endothelial cells in the TME induce macrophage M2 polarization via IL-6 and that depletion of endothelial IL-6 improves survival.
Macrophages in the tumour microenvironment (TME) acquire tumour-promoting functions upon M2 polarization. Here the authors show, in a mouse model of glioblastoma, that endothelial cells in the TME induce macrophage M2 polarization via IL-6 and that depletion of endothelial IL-6 improves survival.
Spatiotemporal regulation of tumor immunity remains largely unexplored. Here we identify a vascular niche that controls alternative macrophage activation in glioblastoma (GBM). We show that tumor-promoting macrophages are spatially proximate to GBM-associated endothelial cells (ECs), permissive for angiocrine-induced macrophage polarization. We identify ECs as one of the major sources for interleukin-6 (IL-6) expression in GBM microenvironment. Furthermore, we reveal that colony-stimulating factor-1 and angiocrine IL-6 induce robust arginase-1 expression and macrophage alternative activation, mediated through peroxisome proliferator-activated receptor-γ-dependent transcriptional activation of hypoxia-inducible factor-2α. Finally, utilizing a genetic murine GBM model, we show that EC-specific knockout of IL-6 inhibits macrophage alternative activation and improves survival in the GBM-bearing mice. These findings illustrate a vascular niche-dependent mechanism for alternative macrophage activation and cancer progression, and suggest that targeting endothelial IL-6 may offer a selective and efficient therapeutic strategy for GBM, and possibly other solid malignant tumors.Spatiotemporal regulation of tumor immunity remains largely unexplored. Here we identify a vascular niche that controls alternative macrophage activation in glioblastoma (GBM). We show that tumor-promoting macrophages are spatially proximate to GBM-associated endothelial cells (ECs), permissive for angiocrine-induced macrophage polarization. We identify ECs as one of the major sources for interleukin-6 (IL-6) expression in GBM microenvironment. Furthermore, we reveal that colony-stimulating factor-1 and angiocrine IL-6 induce robust arginase-1 expression and macrophage alternative activation, mediated through peroxisome proliferator-activated receptor-γ-dependent transcriptional activation of hypoxia-inducible factor-2α. Finally, utilizing a genetic murine GBM model, we show that EC-specific knockout of IL-6 inhibits macrophage alternative activation and improves survival in the GBM-bearing mice. These findings illustrate a vascular niche-dependent mechanism for alternative macrophage activation and cancer progression, and suggest that targeting endothelial IL-6 may offer a selective and efficient therapeutic strategy for GBM, and possibly other solid malignant tumors.
ArticleNumber 559
Author Duan, Hao
Hidalgo, Juan
Ma, Peihong
Wang, Yanling
Gong, Yanqing
Fan, Yi
Zhang, Lin
Huang, Menggui
Dahmane, Nadia
He, Zhenqiang
Zamvil, Scott S.
Wang, Qirui
Xu, Haineng
Brem, Steven
Liu, Tianrun
Mou, Yonggao
Zhang, Zhenfeng
O’Rourke, Donald M.
Author_xml – sequence: 1
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  surname: Wang
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  organization: Department of Radiation Oncology, University of Pennsylvania Perelman School of Medicine, School of Traditional Chinese Medicine, Southern Medical University
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  givenname: Zhenqiang
  surname: He
  fullname: He, Zhenqiang
  organization: Department of Radiation Oncology, University of Pennsylvania Perelman School of Medicine, Department of Neurosurgery, Sun Yat-sen University Cancer Center
– sequence: 3
  givenname: Menggui
  surname: Huang
  fullname: Huang, Menggui
  organization: Department of Radiation Oncology, University of Pennsylvania Perelman School of Medicine
– sequence: 4
  givenname: Tianrun
  surname: Liu
  fullname: Liu, Tianrun
  organization: Department of Radiation Oncology, University of Pennsylvania Perelman School of Medicine, Department of Otorhinolaryngology, Division of Head and Neck Surgery, The Sixth Affiliated Hospital of Sun Yat-sen University
– sequence: 5
  givenname: Yanling
  surname: Wang
  fullname: Wang, Yanling
  organization: Department of Radiation Oncology, University of Pennsylvania Perelman School of Medicine
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  givenname: Haineng
  surname: Xu
  fullname: Xu, Haineng
  organization: Department of Radiation Oncology, University of Pennsylvania Perelman School of Medicine
– sequence: 7
  givenname: Hao
  surname: Duan
  fullname: Duan, Hao
  organization: Department of Radiation Oncology, University of Pennsylvania Perelman School of Medicine, Department of Neurosurgery, Sun Yat-sen University Cancer Center
– sequence: 8
  givenname: Peihong
  surname: Ma
  fullname: Ma, Peihong
  organization: Department of Radiation Oncology, University of Pennsylvania Perelman School of Medicine
– sequence: 9
  givenname: Lin
  orcidid: 0000-0003-1998-0611
  surname: Zhang
  fullname: Zhang, Lin
  organization: Department of Obstetrics and Gynecology, University of Pennsylvania Perelman School of Medicine
– sequence: 10
  givenname: Scott S.
  surname: Zamvil
  fullname: Zamvil, Scott S.
  organization: Department of Neurology and Program in Immunology, University of California at San Francisco
– sequence: 11
  givenname: Juan
  orcidid: 0000-0003-0921-1122
  surname: Hidalgo
  fullname: Hidalgo, Juan
  organization: Department of Cellular Biology, Physiology, and Immunology, Autonomous University of Barcelona
– sequence: 12
  givenname: Zhenfeng
  orcidid: 0000-0001-5621-9755
  surname: Zhang
  fullname: Zhang, Zhenfeng
  organization: Department of Radiology The, Second Affiliated Hospital of Guangzhou Medical University
– sequence: 13
  givenname: Donald M.
  surname: O’Rourke
  fullname: O’Rourke, Donald M.
  organization: Department of Neurosurgery, University of Pennsylvania Perelman School of Medicine
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  givenname: Nadia
  surname: Dahmane
  fullname: Dahmane, Nadia
  organization: Department of Neurosurgery, University of Pennsylvania Perelman School of Medicine
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  givenname: Steven
  surname: Brem
  fullname: Brem, Steven
  organization: Department of Neurosurgery, University of Pennsylvania Perelman School of Medicine
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  surname: Mou
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  organization: Department of Neurosurgery, Sun Yat-sen University Cancer Center
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  givenname: Yanqing
  surname: Gong
  fullname: Gong, Yanqing
  organization: Department of Medicine, Division of Human Genetics and Translational Medicine, University of Pennsylvania Perelman School of Medicine
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  givenname: Yi
  surname: Fan
  fullname: Fan, Yi
  email: fanyi@uphs.upenn.edu
  organization: Department of Radiation Oncology, University of Pennsylvania Perelman School of Medicine, Department of Neurosurgery, University of Pennsylvania Perelman School of Medicine
BackLink https://www.ncbi.nlm.nih.gov/pubmed/29422647$$D View this record in MEDLINE/PubMed
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Snippet Spatiotemporal regulation of tumor immunity remains largely unexplored. Here we identify a vascular niche that controls alternative macrophage activation in...
Macrophages in the tumour microenvironment (TME) acquire tumour-promoting functions upon M2 polarization. Here the authors show, in a mouse model of...
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SubjectTerms 13/31
14/5
45/77
45/88
45/90
631/67/1922
631/67/327
64/110
96/1
Animals
Arginase
Arginase - immunology
Basic Helix-Loop-Helix Transcription Factors - genetics
Brain cancer
Cancer
Cancer therapies
Cell activation
Cell Line, Tumor
Cells, Cultured
Colony-stimulating factor
Cytokines
Disease Progression
Endothelial cells
Endothelial Cells - immunology
Flow cytometry
Glioblastoma
Glioblastoma - immunology
Growth factors
Human subjects
Humanities and Social Sciences
Humans
Hypoxia
Hypoxia-inducible factors
Immunity
Immunology
Interleukin 6
Interleukin-6 - immunology
Macrophage Activation - immunology
Macrophage colony-stimulating factor
Macrophage Colony-Stimulating Factor - immunology
Macrophages
Macrophages - immunology
Medicine
Mice
Microvessels - cytology
Monocytes - immunology
multidisciplinary
Neoplasms, Experimental - immunology
Neurosurgery
Nitric oxide
Otolaryngology
Peroxisome proliferator-activated receptors
Polarization
Polyamines
Radiation
Rodents
Science
Science (multidisciplinary)
Survival
Transcription activation
Transcriptional Activation
Tumor Microenvironment
Tumors
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Title Vascular niche IL-6 induces alternative macrophage activation in glioblastoma through HIF-2α
URI https://link.springer.com/article/10.1038/s41467-018-03050-0
https://www.ncbi.nlm.nih.gov/pubmed/29422647
https://www.proquest.com/docview/1999660218
https://www.proquest.com/docview/2913314148
https://www.proquest.com/docview/2001065373
https://pubmed.ncbi.nlm.nih.gov/PMC5805734
https://doaj.org/article/5f37ad77abf54c4e89ce8111d4283ac7
Volume 9
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