IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-33235-7.html
   My bibliography  Save this article

Angiocrine extracellular vesicles impose mesenchymal reprogramming upon proneural glioma stem cells

Author

Listed:
  • Lata Adnani

    (Research Institute of the McGill University Health Centre)

  • Jordan Kassouf

    (McGill University)

  • Brian Meehan

    (Research Institute of the McGill University Health Centre)

  • Cristiana Spinelli

    (Research Institute of the McGill University Health Centre)

  • Nadim Tawil

    (Research Institute of the McGill University Health Centre)

  • Ichiro Nakano

    (Hokuto Hospital)

  • Janusz Rak

    (Research Institute of the McGill University Health Centre
    McGill University)

Abstract

Glioblastoma (GBM) is an incurable form of primary astrocytic brain tumor driven by glioma stem cell (GSC) compartment closely associated with the vascular niche. GSC phenotypes are heterogeneous and range from proneural to mesenchymal-like, the latter characterised by greater invasiveness. Here we document the secretory (angiocrine) role of endothelial cells and their derived extracellular vesicles (EVs) as drivers of proneural-to-mesenchymal reprogramming of GSCs. These changes involve activation of matrix metalloproteinases (MMPs) and NFκB, and inactivation of NOTCH, while altering responsiveness to chemotherapy and driving infiltrative growth in the brain. Our findings suggest that EV-mediated angiocrine interactions impact the nature of cellular stemness in GBM with implications for disease biology and therapy.

Suggested Citation

  • Lata Adnani & Jordan Kassouf & Brian Meehan & Cristiana Spinelli & Nadim Tawil & Ichiro Nakano & Janusz Rak, 2022. "Angiocrine extracellular vesicles impose mesenchymal reprogramming upon proneural glioma stem cells," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33235-7
    DOI: 10.1038/s41467-022-33235-7
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-33235-7
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-33235-7?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Lucia Ricci-Vitiani & Roberto Pallini & Mauro Biffoni & Matilde Todaro & Gloria Invernici & Tonia Cenci & Giulio Maira & Eugenio Agostino Parati & Giorgio Stassi & Luigi Maria Larocca & Ruggero De Mar, 2010. "Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells," Nature, Nature, vol. 468(7325), pages 824-828, December.
    2. Luigi Ombrato & Emma Nolan & Ivana Kurelac & Antranik Mavousian & Victoria Louise Bridgeman & Ivonne Heinze & Probir Chakravarty & Stuart Horswell & Estela Gonzalez-Gualda & Giulia Matacchione & Anne , 2019. "Author Correction: Metastatic-niche labelling reveals parenchymal cells with stem features," Nature, Nature, vol. 575(7784), pages 8-8, November.
    3. Rong Wang & Kalyani Chadalavada & Jennifer Wilshire & Urszula Kowalik & Koos E. Hovinga & Adam Geber & Boris Fligelman & Margaret Leversha & Cameron Brennan & Viviane Tabar, 2010. "Glioblastoma stem-like cells give rise to tumour endothelium," Nature, Nature, vol. 468(7325), pages 829-833, December.
    4. Soniya Bastola & Marat S. Pavlyukov & Daisuke Yamashita & Sadashib Ghosh & Heejin Cho & Noritaka Kagaya & Zhuo Zhang & Mutsuko Minata & Yeri Lee & Hirokazu Sadahiro & Shinobu Yamaguchi & Svetlana Koma, 2020. "Glioma-initiating cells at tumor edge gain signals from tumor core cells to promote their malignancy," Nature Communications, Nature, vol. 11(1), pages 1-17, December.
    5. Erik Jung & Matthias Osswald & Miriam Ratliff & Helin Dogan & Ruifan Xie & Sophie Weil & Dirk C. Hoffmann & Felix T. Kurz & Tobias Kessler & Sabine Heiland & Andreas Deimling & Felix Sahm & Wolfgang W, 2021. "Tumor cell plasticity, heterogeneity, and resistance in crucial microenvironmental niches in glioma," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Eunnyung Bae & Ping Huang & Gaёlle Müller-Greven & Dolores Hambardzumyan & Andrew Edward Sloan & Amy S. Nowacki & Nicholas Marko & Cathleen R. Carlin & Candece L. Gladson, 2022. "Integrin α3β1 promotes vessel formation of glioblastoma-associated endothelial cells through calcium-mediated macropinocytosis and lysosomal exocytosis," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Sree Deepthi Muthukrishnan & Riki Kawaguchi & Pooja Nair & Rachna Prasad & Yue Qin & Maverick Johnson & Qing Wang & Nathan VanderVeer-Harris & Amy Pham & Alvaro G. Alvarado & Michael C. Condro & Fuyin, 2022. "P300 promotes tumor recurrence by regulating radiation-induced conversion of glioma stem cells to vascular-like cells," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    3. Cristiana Spinelli & Lata Adnani & Brian Meehan & Laura Montermini & Sidong Huang & Minjun Kim & Tamiko Nishimura & Sidney E. Croul & Ichiro Nakano & Yasser Riazalhosseini & Janusz Rak, 2024. "Mesenchymal glioma stem cells trigger vasectasia—distinct neovascularization process stimulated by extracellular vesicles carrying EGFR," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    4. Bingjie Guan & Youdong Liu & Bowen Xie & Senlin Zhao & Abudushalamu Yalikun & Weiwei Chen & Menghua Zhou & Qi Gu & Dongwang Yan, 2024. "Mitochondrial genome transfer drives metabolic reprogramming in adjacent colonic epithelial cells promoting TGFβ1-mediated tumor progression," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    5. Anna Cioce & Beatriz Calle & Tatiana Rizou & Sarah C. Lowery & Victoria L. Bridgeman & Keira E. Mahoney & Andrea Marchesi & Ganka Bineva-Todd & Helen Flynn & Zhen Li & Omur Y. Tastan & Chloe Roustan &, 2022. "Cell-specific bioorthogonal tagging of glycoproteins," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    6. Marc Cicero Schubert & Stella Judith Soyka & Amr Tamimi & Emanuel Maus & Julian Schroers & Niklas Wißmann & Ekin Reyhan & Svenja Kristin Tetzlaff & Yvonne Yang & Robert Denninger & Robin Peretzke & Ca, 2024. "Deep intravital brain tumor imaging enabled by tailored three-photon microscopy and analysis," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    7. Yan Zou & Yajing Sun & Yibin Wang & Dongya Zhang & Huiqing Yang & Xin Wang & Meng Zheng & Bingyang Shi, 2023. "Cancer cell-mitochondria hybrid membrane coated Gboxin loaded nanomedicines for glioblastoma treatment," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    8. Misa Minegishi & Takahiro Kuchimaru & Kaori Nishikawa & Takayuki Isagawa & Satoshi Iwano & Kei Iida & Hiromasa Hara & Shizuka Miura & Marika Sato & Shigeaki Watanabe & Akifumi Shiomi & Yo Mabuchi & Hi, 2023. "Secretory GFP reconstitution labeling of neighboring cells interrogates cell–cell interactions in metastatic niches," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    9. Ling Hai & Dirk C. Hoffmann & Robin J. Wagener & Daniel D. Azorin & David Hausmann & Ruifan Xie & Magnus-Carsten Huppertz & Julien Hiblot & Philipp Sievers & Sophie Heuer & Jakob Ito & Gina Cebulla & , 2024. "A clinically applicable connectivity signature for glioblastoma includes the tumor network driver CHI3L1," Nature Communications, Nature, vol. 15(1), pages 1-29, December.
    10. Ting Xie & Adi Danieli-Mackay & Mariachiara Buccarelli & Mariano Barbieri & Ioanna Papadionysiou & Q. Giorgio D’Alessandris & Claudia Robens & Nadine Übelmesser & Omkar Suhas Vinchure & Liverana Laure, 2024. "Pervasive structural heterogeneity rewires glioblastoma chromosomes to sustain patient-specific transcriptional programs," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    11. Yun Chang & Xuechao Cai & Ramizah Syahirah & Yuxing Yao & Yang Xu & Gyuhyung Jin & Vijesh J. Bhute & Sandra Torregrosa-Allen & Bennett D. Elzey & You-Yeon Won & Qing Deng & Xiaojun Lance Lian & Xiaogu, 2023. "CAR-neutrophil mediated delivery of tumor-microenvironment responsive nanodrugs for glioblastoma chemo-immunotherapy," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    12. Jing Huang & Weijun Huang & Junzhe Yi & Yiwen Deng & Ruijie Li & Jieying Chen & Jiahao Shi & Yuan Qiu & Tao Wang & Xiaoyong Chen & Xiaoran Zhang & Andy Peng Xiang, 2023. "Mesenchymal stromal cells alleviate depressive and anxiety-like behaviors via a lung vagal-to-brain axis in male mice," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    13. Kristina Handler & Karsten Bach & Costanza Borrelli & Salvatore Piscuoglio & Xenia Ficht & Ilhan E. Acar & Andreas E. Moor, 2023. "Fragment-sequencing unveils local tissue microenvironments at single-cell resolution," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    14. Guiraldello, Rafael T. & Martins, Marcelo L. & Mancera, Paulo F.A., 2016. "Evaluating the efficacies of Maximum Tolerated Dose and metronomic chemotherapies: A mathematical approach," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 456(C), pages 145-156.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33235-7. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.