A novel neuronal organoid model mimicking glioblastoma (GBM) features from induced pluripotent stem cells (iPSC).


Journal

Biochimica et biophysica acta. General subjects
ISSN: 1872-8006
Titre abrégé: Biochim Biophys Acta Gen Subj
Pays: Netherlands
ID NLM: 101731726

Informations de publication

Date de publication:
04 2020
Historique:
received: 03 09 2019
revised: 07 01 2020
accepted: 17 01 2020
pubmed: 25 1 2020
medline: 15 9 2020
entrez: 25 1 2020
Statut: ppublish

Résumé

Current experimental models using either human or mouse cell lines, are not representative of the complex features of GBM. In particular, there is no model to study patient-derived iPSCs to generate a GBM model. Overexpression of c-met gene is one of the molecular features of GBM leading to increased signaling via STAT3 phosphorylation. We generated an iPSC line from a patient with c-met mutation and we asked whether we could use it to generate neuronal-like organoids mimicking features of GBM. We have generated iPSC-aggregates differentiating towards organoids. We analyzed them by gene expression profiling, immunostaining and transmission electronic microscopy analyses (TEM). Herein we describe that c-met-mutated iPSC aggregates spontaneously differentiate into dopaminergic neurons more rapidly than control iPSC aggregates in culture. Gene expression profiling of c-met-mutated iPSC aggregates at day +90 showed neuronal- and GBM-related genes, reproducing a genomic network described in primary human GBM. Comparative TEM analyses confirmed the enrichment of these structures in intermediate filaments and abnormal cilia, a feature described in human GBM. The c-met-mutated iPSC-derived organoids, as compared to controls expressed high levels of glial fibrillary acidic protein (GFAP), which is a typical marker of human GBM, as well as high levels of phospho-MET and phospho-STAT3. The use of temozolomide (TMZ) showed a preferential cytotoxicity of this drug in c-met-mutated neuronal-like organoids. This study shows the feasibility of generating "off-the shelf" neuronal-like organoid model mimicking GBM using c-met-mutated iPSC aggregates and its potential future use in research.

Sections du résumé

BACKGROUND
Current experimental models using either human or mouse cell lines, are not representative of the complex features of GBM. In particular, there is no model to study patient-derived iPSCs to generate a GBM model. Overexpression of c-met gene is one of the molecular features of GBM leading to increased signaling via STAT3 phosphorylation. We generated an iPSC line from a patient with c-met mutation and we asked whether we could use it to generate neuronal-like organoids mimicking features of GBM.
METHODS
We have generated iPSC-aggregates differentiating towards organoids. We analyzed them by gene expression profiling, immunostaining and transmission electronic microscopy analyses (TEM).
RESULTS
Herein we describe that c-met-mutated iPSC aggregates spontaneously differentiate into dopaminergic neurons more rapidly than control iPSC aggregates in culture. Gene expression profiling of c-met-mutated iPSC aggregates at day +90 showed neuronal- and GBM-related genes, reproducing a genomic network described in primary human GBM. Comparative TEM analyses confirmed the enrichment of these structures in intermediate filaments and abnormal cilia, a feature described in human GBM. The c-met-mutated iPSC-derived organoids, as compared to controls expressed high levels of glial fibrillary acidic protein (GFAP), which is a typical marker of human GBM, as well as high levels of phospho-MET and phospho-STAT3. The use of temozolomide (TMZ) showed a preferential cytotoxicity of this drug in c-met-mutated neuronal-like organoids.
GENERAL SIGNIFICANCE
This study shows the feasibility of generating "off-the shelf" neuronal-like organoid model mimicking GBM using c-met-mutated iPSC aggregates and its potential future use in research.

Identifiants

pubmed: 31978452
pii: S0304-4165(20)30030-1
doi: 10.1016/j.bbagen.2020.129540
pii:
doi:

Substances chimiques

Temozolomide YF1K15M17Y

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

129540

Informations de copyright

Copyright © 2020 Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Competing Interest The authors declare no conflicts of interest.

Auteurs

Jin Wook Hwang (JW)

INSERM UMR-S 935, Université Paris Sud, 94800 Villejuif, France; ESTeam Paris Sud, Université Paris Sud, 94800 Villejuif, France.

Julien Loisel-Duwattez (J)

INSERM U1195, Université Paris Sud, Faculté de Médecine, APHP, Service de Neurologie, Bicêtre Hospital, 94276 le Kremlin Bicêtre, France.

Christophe Desterke (C)

INSERM UMR-S 935, Université Paris Sud, 94800 Villejuif, France; ESTeam Paris Sud, Université Paris Sud, 94800 Villejuif, France.

Theodoros Latsis (T)

INSERM UMR-S 935, Université Paris Sud, 94800 Villejuif, France; ESTeam Paris Sud, Université Paris Sud, 94800 Villejuif, France.

Sarah Pagliaro (S)

INSERM UMR-S 935, Université Paris Sud, 94800 Villejuif, France; ESTeam Paris Sud, Université Paris Sud, 94800 Villejuif, France.

Frank Griscelli (F)

INSERM UMR-S 935, Université Paris Sud, 94800 Villejuif, France; ESTeam Paris Sud, Université Paris Sud, 94800 Villejuif, France.

Annelise Bennaceur-Griscelli (A)

INSERM UMR-S 935, Université Paris Sud, 94800 Villejuif, France.

Ali G Turhan (AG)

INSERM UMR-S 935, Université Paris Sud, 94800 Villejuif, France; INGESTEM National IPSC Infrastructure, 94800 Villejuif, France; Division of Hematology, Paris Sud University Hospitals, Le Kremlin Bicêtre 75006, Villejuif 94800, France; ESTeam Paris Sud, Université Paris Sud, 94800 Villejuif, France. Electronic address: turviv33@gmail.com.

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Classifications MeSH