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Tumor-associated reactive astrocytes aid the evolution of immunosuppressive environment in glioblastoma

Author

Listed:
  • Dieter Henrik Heiland

    (University of Freiburg
    University of Freiburg
    Freiburg University)

  • Vidhya M. Ravi

    (University of Freiburg
    Freiburg University
    University of Freiburg)

  • Simon P. Behringer

    (University of Freiburg
    University of Freiburg
    Freiburg University)

  • Jan Hendrik Frenking

    (University of Freiburg
    University of Freiburg
    Freiburg University)

  • Julian Wurm

    (University of Freiburg
    University of Freiburg
    Freiburg University)

  • Kevin Joseph

    (University of Freiburg
    Freiburg University
    University of Freiburg)

  • Nicklas W. C. Garrelfs

    (University of Freiburg
    University of Freiburg
    Freiburg University)

  • Jakob Strähle

    (University of Freiburg
    Freiburg University)

  • Sabrina Heynckes

    (University of Freiburg
    University of Freiburg
    Freiburg University)

  • Jürgen Grauvogel

    (University of Freiburg
    Freiburg University)

  • Pamela Franco

    (University of Freiburg
    University of Freiburg
    Freiburg University)

  • Irina Mader

    (University of Freiburg
    Epilepsy Center for Children and Adolescents)

  • Matthias Schneider

    (University of Bonn)

  • Anna-Laura Potthoff

    (University of Bonn)

  • Daniel Delev

    (University of Aachen)

  • Ulrich G. Hofmann

    (University of Freiburg
    Freiburg University
    University of Freiburg)

  • Christian Fung

    (University of Freiburg
    Freiburg University)

  • Jürgen Beck

    (University of Freiburg
    Freiburg University)

  • Roman Sankowski

    (Freiburg University
    University of Freiburg)

  • Marco Prinz

    (Freiburg University
    University of Freiburg
    University of Freiburg
    University of Freiburg)

  • Oliver Schnell

    (University of Freiburg
    University of Freiburg
    Freiburg University)

Abstract

Reactive astrocytes evolve after brain injury, inflammatory and degenerative diseases, whereby they undergo transcriptomic re-programming. In malignant brain tumors, their function and crosstalk to other components of the environment is poorly understood. Here we report a distinct transcriptional phenotype of reactive astrocytes from glioblastoma linked to JAK/STAT pathway activation. Subsequently, we investigate the origin of astrocytic transformation by a microglia loss-of-function model in a human organotypic slice model with injected tumor cells. RNA-seq based gene expression analysis of astrocytes reveals a distinct astrocytic phenotype caused by the coexistence of microglia and astrocytes in the tumor environment, which leads to a large release of anti-inflammatory cytokines such as TGFβ, IL10 and G-CSF. Inhibition of the JAK/STAT pathway shifts the balance of pro- and anti-inflammatory cytokines towards a pro-inflammatory environment. The complex interaction of astrocytes and microglia cells promotes an immunosuppressive environment, suggesting that tumor-associated astrocytes contribute to anti-inflammatory responses.

Suggested Citation

  • Dieter Henrik Heiland & Vidhya M. Ravi & Simon P. Behringer & Jan Hendrik Frenking & Julian Wurm & Kevin Joseph & Nicklas W. C. Garrelfs & Jakob Strähle & Sabrina Heynckes & Jürgen Grauvogel & Pamela , 2019. "Tumor-associated reactive astrocytes aid the evolution of immunosuppressive environment in glioblastoma," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-10493-6
    DOI: 10.1038/s41467-019-10493-6
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    Cited by:

    1. Qi Zhang & Rober Abdo & Cristiana Iosef & Tomonori Kaneko & Matthew Cecchini & Victor K. Han & Shawn Shun-Cheng Li, 2022. "The spatial transcriptomic landscape of non-small cell lung cancer brain metastasis," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    2. Xiaojing Shi & Longlong Luo & Jixian Wang & Hui Shen & Yongfang Li & Muyassar Mamtilahun & Chang Liu & Rubing Shi & Joon-Hyuk Lee & Hengli Tian & Zhijun Zhang & Yongting Wang & Won-Suk Chung & Yaohui , 2021. "Stroke subtype-dependent synapse elimination by reactive gliosis in mice," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
    3. Xianhui Ruan & Wei Yan & Minghui Cao & Ray Anthony M. Daza & Miranda Y. Fong & Kaifu Yang & Jun Wu & Xuxiang Liu & Melanie Palomares & Xiwei Wu & Arthur Li & Yuan Chen & Rahul Jandial & Nicholas C. Sp, 2024. "Breast cancer cell-secreted miR-199b-5p hijacks neurometabolic coupling to promote brain metastasis," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    4. Osama Al-Dalahmah & Michael G. Argenziano & Adithya Kannan & Aayushi Mahajan & Julia Furnari & Fahad Paryani & Deborah Boyett & Akshay Save & Nelson Humala & Fatima Khan & Juncheng Li & Hong Lu & Yu S, 2023. "Re-convolving the compositional landscape of primary and recurrent glioblastoma reveals prognostic and targetable tissue states," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    5. Yuanning Zheng & Francisco Carrillo-Perez & Marija Pizurica & Dieter Henrik Heiland & Olivier Gevaert, 2023. "Spatial cellular architecture predicts prognosis in glioblastoma," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    6. Vidhya M. Ravi & Nicolas Neidert & Paulina Will & Kevin Joseph & Julian P. Maier & Jan Kückelhaus & Lea Vollmer & Jonathan M. Goeldner & Simon P. Behringer & Florian Scherer & Melanie Boerries & Marie, 2022. "T-cell dysfunction in the glioblastoma microenvironment is mediated by myeloid cells releasing interleukin-10," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    7. Mathias Linnerbauer & Tobias Beyer & Lucy Nirschl & Daniel Farrenkopf & Lena Lößlein & Oliver Vandrey & Anne Peter & Thanos Tsaktanis & Hania Kebir & David Laplaud & Rupert Oellinger & Thomas Engleitn, 2023. "PD-L1 positive astrocytes attenuate inflammatory functions of PD-1 positive microglia in models of autoimmune neuroinflammation," Nature Communications, Nature, vol. 14(1), pages 1-17, December.

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