An extracellular vesicle-related gene expression signature identifies high-risk patients in medulloblastoma.

extracellular vesicle gene expression signature medulloblastoma single-cell RNA sequencing tumor microenvironment

Journal

Neuro-oncology
ISSN: 1523-5866
Titre abrégé: Neuro Oncol
Pays: England
ID NLM: 100887420

Informations de publication

Date de publication:
12 04 2021
Historique:
pubmed: 12 11 2020
medline: 21 5 2021
entrez: 11 11 2020
Statut: ppublish

Résumé

Medulloblastoma (MB) is a malignant brain tumor in childhood. It comprises 4 subgroups with different clinical behaviors. The aim of this study was to characterize the transcriptomic landscape of MB, both at the level of individual tumors as well as in large patient cohorts. We used a combination of single-cell transcriptomics, cell culture models and biophysical methods such as nanoparticle tracking analysis and electron microscopy to investigate intercellular communication in the MB tumor niche. Tumor cells of the sonic hedgehog (SHH)-MB subgroup show a differentiation blockade. These cells undergo extensive metabolic reprogramming. The gene expression profiles of individual tumor cells show a partial convergence with those of tumor-associated glial and immune cells. One possible cause is the transfer of extracellular vesicles (EVs) between cells in the tumor niche. We were able to detect EVs in co-culture models of MB tumor cells and oligodendrocytes. We also identified a gene expression signature, EVS, which shows overlap with the proteome profile of large oncosomes from prostate cancer cells. This signature is also present in MB patient samples. A high EVS expression is one common characteristic of tumors that occur in high-risk patients from different MB subgroups or subtypes. With EVS, our study uncovered a novel gene expression signature that has a high prognostic significance across MB subgroups.

Sections du résumé

BACKGROUND
Medulloblastoma (MB) is a malignant brain tumor in childhood. It comprises 4 subgroups with different clinical behaviors. The aim of this study was to characterize the transcriptomic landscape of MB, both at the level of individual tumors as well as in large patient cohorts.
METHODS
We used a combination of single-cell transcriptomics, cell culture models and biophysical methods such as nanoparticle tracking analysis and electron microscopy to investigate intercellular communication in the MB tumor niche.
RESULTS
Tumor cells of the sonic hedgehog (SHH)-MB subgroup show a differentiation blockade. These cells undergo extensive metabolic reprogramming. The gene expression profiles of individual tumor cells show a partial convergence with those of tumor-associated glial and immune cells. One possible cause is the transfer of extracellular vesicles (EVs) between cells in the tumor niche. We were able to detect EVs in co-culture models of MB tumor cells and oligodendrocytes. We also identified a gene expression signature, EVS, which shows overlap with the proteome profile of large oncosomes from prostate cancer cells. This signature is also present in MB patient samples. A high EVS expression is one common characteristic of tumors that occur in high-risk patients from different MB subgroups or subtypes.
CONCLUSIONS
With EVS, our study uncovered a novel gene expression signature that has a high prognostic significance across MB subgroups.

Identifiants

pubmed: 33175161
pii: 5974128
doi: 10.1093/neuonc/noaa254
pmc: PMC8041350
doi:

Substances chimiques

Hedgehog Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

586-598

Commentaires et corrections

Type : CommentIn

Informations de copyright

© The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Neuro-Oncology. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.

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Auteurs

Thomas K Albert (TK)

Department of Pediatric Hematology and Oncology, University Children's Hospital Münster, Münster, Germany.

Marta Interlandi (M)

Department of Pediatric Hematology and Oncology, University Children's Hospital Münster, Münster, Germany.
Institute of Medical Informatics, Westphalian-Wilhelms-University (WWU) Münster, Münster, Germany.

Martin Sill (M)

Hopp-Children's Cancer Center at the NCT Heidelberg (KiTZ), Heidelberg, Germany.
Division of Pediatric Neurooncology, German Cancer Research Center (DKFZ), Heidelberg, Germany.

Monika Graf (M)

Department of Pediatric Hematology and Oncology, University Children's Hospital Münster, Münster, Germany.

Natalia Moreno (N)

Department of Pediatric Hematology and Oncology, University Children's Hospital Münster, Münster, Germany.

Kerstin Menck (K)

Department of Medicine A, Hematology, Oncology, and Pneumology, University Hospital Münster (UKM), Münster, Germany.

Astrid Rohlmann (A)

Department of Medicine A, Hematology, Oncology, and Pneumology, University Hospital Münster (UKM), Münster, Germany.
Department of Anatomy and Molecular Neurobiology, WWU Münster, Münster, Germany.

Viktoria Melcher (V)

Department of Pediatric Hematology and Oncology, University Children's Hospital Münster, Münster, Germany.

Sonja Korbanka (S)

Department of Pediatric Hematology and Oncology, University Children's Hospital Münster, Münster, Germany.

Gerd Meyer Zu Hörste (G)

Department of Neurology, UKM, Münster, Germany.

Tobias Lautwein (T)

Biological and Medical Research Center, Heinrich Heine University Düsseldorf, Düsseldorf, Germany.

Michael C Frühwald (MC)

Swabian Children's Cancer Center, Children's Hospital Augsburg, Augsburg, Germany.

Christian F Krebs (CF)

Center for Internal Medicine, III. Medical Clinic and Polyclinic, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Dörthe Holdhof (D)

Department of Pediatric Hematology and Oncology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
Research Institute Children's Cancer Center, Hamburg, Germany.

Melanie Schoof (M)

Department of Pediatric Hematology and Oncology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
Research Institute Children's Cancer Center, Hamburg, Germany.

Annalen Bleckmann (A)

Department of Medicine A, Hematology, Oncology, and Pneumology, University Hospital Münster (UKM), Münster, Germany.

Markus Missler (M)

Department of Anatomy and Molecular Neurobiology, WWU Münster, Münster, Germany.

Martin Dugas (M)

Institute of Medical Informatics, Westphalian-Wilhelms-University (WWU) Münster, Münster, Germany.

Ulrich Schüller (U)

Department of Pediatric Hematology and Oncology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
Research Institute Children's Cancer Center, Hamburg, Germany.
Institute of Neuropathology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Natalie Jäger (N)

Hopp-Children's Cancer Center at the NCT Heidelberg (KiTZ), Heidelberg, Germany.

Stefan M Pfister (SM)

Hopp-Children's Cancer Center at the NCT Heidelberg (KiTZ), Heidelberg, Germany.
Division of Pediatric Neurooncology, German Cancer Research Center (DKFZ), Heidelberg, Germany.
German Cancer Consortium (DKTK) Heidelberg, Heidelberg, Germany.
Department of Pediatric Oncology, Hematology and Immunology, University Hospital Heidelberg, Heidelberg, Germany.

Kornelius Kerl (K)

Department of Pediatric Hematology and Oncology, University Children's Hospital Münster, Münster, Germany.

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