Single-nucleus and spatial landscape of the sub-ventricular zone in human glioblastoma

Summary: The sub-ventricular zone (SVZ) is the most well-characterized neurogenic area in the mammalian brain. We previously showed that in 65% of patients with glioblastoma (GBM), the SVZ is a reservoir of cancer stem-like cells that contribute to treatment resistance and the emergence of recurrenc...

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Main Authors: Yamhilette Licón-Muñoz, Vanessa Avalos, Suganya Subramanian, Bryan Granger, Frank Martinez, Leopoldo A. García-Montaño, Samantha Varela, Drew Moore, Eddie Perkins, Michael Kogan, Stefano Berto, Muhammad O. Chohan, Christian A. Bowers, Sara G.M. Piccirillo
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Cell Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2211124724015006
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author Yamhilette Licón-Muñoz
Vanessa Avalos
Suganya Subramanian
Bryan Granger
Frank Martinez
Leopoldo A. García-Montaño
Samantha Varela
Drew Moore
Eddie Perkins
Michael Kogan
Stefano Berto
Muhammad O. Chohan
Christian A. Bowers
Sara G.M. Piccirillo
author_facet Yamhilette Licón-Muñoz
Vanessa Avalos
Suganya Subramanian
Bryan Granger
Frank Martinez
Leopoldo A. García-Montaño
Samantha Varela
Drew Moore
Eddie Perkins
Michael Kogan
Stefano Berto
Muhammad O. Chohan
Christian A. Bowers
Sara G.M. Piccirillo
author_sort Yamhilette Licón-Muñoz
collection DOAJ
description Summary: The sub-ventricular zone (SVZ) is the most well-characterized neurogenic area in the mammalian brain. We previously showed that in 65% of patients with glioblastoma (GBM), the SVZ is a reservoir of cancer stem-like cells that contribute to treatment resistance and the emergence of recurrence. Here, we build a single-nucleus RNA-sequencing-based microenvironment landscape of the tumor mass and the SVZ of 15 patients and two histologically normal SVZ samples as controls. We identify a ZEB1-centered mesenchymal signature in the tumor cells of the SVZ. Moreover, the SVZ microenvironment is characterized by tumor-supportive microglia, which spatially coexist and establish crosstalks with tumor cells. Last, differential gene expression analyses, predictions of ligand-receptor and incoming/outgoing interactions, and functional assays reveal that the interleukin (IL)-1β/IL-1RAcP and Wnt-5a/Frizzled-3 pathways represent potential therapeutic targets in the SVZ. Our data provide insights into the biology of the SVZ in patients with GBM and identify potential targets of this microenvironment.
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spelling doaj-art-45f20f380bac43cfbe3b0ea40238e2772025-08-20T02:26:14ZengElsevierCell Reports2211-12472025-01-0144111514910.1016/j.celrep.2024.115149Single-nucleus and spatial landscape of the sub-ventricular zone in human glioblastomaYamhilette Licón-Muñoz0Vanessa Avalos1Suganya Subramanian2Bryan Granger3Frank Martinez4Leopoldo A. García-Montaño5Samantha Varela6Drew Moore7Eddie Perkins8Michael Kogan9Stefano Berto10Muhammad O. Chohan11Christian A. Bowers12Sara G.M. Piccirillo13The Brain Tumor Translational Laboratory, Department of Cell Biology and Physiology, University of New Mexico Health Sciences Center, Albuquerque, NM 87131, USA; University of New Mexico Comprehensive Cancer Center, Albuquerque, NM 87131, USAThe Brain Tumor Translational Laboratory, Department of Cell Biology and Physiology, University of New Mexico Health Sciences Center, Albuquerque, NM 87131, USA; University of New Mexico Comprehensive Cancer Center, Albuquerque, NM 87131, USABioinformatics Core, Department of Neuroscience, Medical University of South Carolina, Charleston, SC 29425, USA; Neurogenomics Laboratory, Department of Neuroscience, Medical University of South Carolina, Charleston, SC 29425, USABioinformatics Core, Department of Neuroscience, Medical University of South Carolina, Charleston, SC 29425, USA; Neurogenomics Laboratory, Department of Neuroscience, Medical University of South Carolina, Charleston, SC 29425, USAThe Brain Tumor Translational Laboratory, Department of Cell Biology and Physiology, University of New Mexico Health Sciences Center, Albuquerque, NM 87131, USA; University of New Mexico Comprehensive Cancer Center, Albuquerque, NM 87131, USAThe Brain Tumor Translational Laboratory, Department of Cell Biology and Physiology, University of New Mexico Health Sciences Center, Albuquerque, NM 87131, USA; University of New Mexico Comprehensive Cancer Center, Albuquerque, NM 87131, USAUniversity of New Mexico School of Medicine, Albuquerque, NM 87131, USABioinformatics Core, Department of Neuroscience, Medical University of South Carolina, Charleston, SC 29425, USA; Neurogenomics Laboratory, Department of Neuroscience, Medical University of South Carolina, Charleston, SC 29425, USADepartment of Neurosurgery, University of Mississippi Medical Center, Jackson, MS 39216, USADepartment of Neurosurgery, University of New Mexico Hospital, Albuquerque, NM 87131, USABioinformatics Core, Department of Neuroscience, Medical University of South Carolina, Charleston, SC 29425, USA; Neurogenomics Laboratory, Department of Neuroscience, Medical University of South Carolina, Charleston, SC 29425, USADepartment of Neurosurgery, University of Mississippi Medical Center, Jackson, MS 39216, USADepartment of Neurosurgery, University of New Mexico Hospital, Albuquerque, NM 87131, USAThe Brain Tumor Translational Laboratory, Department of Cell Biology and Physiology, University of New Mexico Health Sciences Center, Albuquerque, NM 87131, USA; University of New Mexico Comprehensive Cancer Center, Albuquerque, NM 87131, USA; Corresponding authorSummary: The sub-ventricular zone (SVZ) is the most well-characterized neurogenic area in the mammalian brain. We previously showed that in 65% of patients with glioblastoma (GBM), the SVZ is a reservoir of cancer stem-like cells that contribute to treatment resistance and the emergence of recurrence. Here, we build a single-nucleus RNA-sequencing-based microenvironment landscape of the tumor mass and the SVZ of 15 patients and two histologically normal SVZ samples as controls. We identify a ZEB1-centered mesenchymal signature in the tumor cells of the SVZ. Moreover, the SVZ microenvironment is characterized by tumor-supportive microglia, which spatially coexist and establish crosstalks with tumor cells. Last, differential gene expression analyses, predictions of ligand-receptor and incoming/outgoing interactions, and functional assays reveal that the interleukin (IL)-1β/IL-1RAcP and Wnt-5a/Frizzled-3 pathways represent potential therapeutic targets in the SVZ. Our data provide insights into the biology of the SVZ in patients with GBM and identify potential targets of this microenvironment.http://www.sciencedirect.com/science/article/pii/S2211124724015006CP: Cancer
spellingShingle Yamhilette Licón-Muñoz
Vanessa Avalos
Suganya Subramanian
Bryan Granger
Frank Martinez
Leopoldo A. García-Montaño
Samantha Varela
Drew Moore
Eddie Perkins
Michael Kogan
Stefano Berto
Muhammad O. Chohan
Christian A. Bowers
Sara G.M. Piccirillo
Single-nucleus and spatial landscape of the sub-ventricular zone in human glioblastoma
Cell Reports
CP: Cancer
title Single-nucleus and spatial landscape of the sub-ventricular zone in human glioblastoma
title_full Single-nucleus and spatial landscape of the sub-ventricular zone in human glioblastoma
title_fullStr Single-nucleus and spatial landscape of the sub-ventricular zone in human glioblastoma
title_full_unstemmed Single-nucleus and spatial landscape of the sub-ventricular zone in human glioblastoma
title_short Single-nucleus and spatial landscape of the sub-ventricular zone in human glioblastoma
title_sort single nucleus and spatial landscape of the sub ventricular zone in human glioblastoma
topic CP: Cancer
url http://www.sciencedirect.com/science/article/pii/S2211124724015006
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