Regulation of glioblastoma stem cells by retinoic acid: role for Notch pathway inhibition

Ying, M; Wang, S; Sang, Y; Sun, P; Lal, B; Goodwin, C R; Guerrero-Cazares, H; Quinones-Hinojosa, A; Laterra, J; Xia, S

doi:10.1038/onc.2011.58

Cited by 204Glioma Diagnosis and TreatmentCancer Cells and MetastasisNeurogenesis and neuroplasticity mechanisms

Regulation of glioblastoma stem cells by retinoic acid: role for Notch pathway inhibition

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Ying, M, Wang, S, Sang, Y, Sun, P, Lal, B, Goodwin, C R, Guerrero-Cazares, H, Quinones-Hinojosa, A +2 more·2011·Oncogene

DOI 10.1038/onc.2011.58PMC PMC3955956

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Abstract

It is necessary to understand mechanisms by which differentiating agents influence tumor-initiating cancer stem cells. Toward this end, we investigated the cellular and molecular responses of glioblastoma stem-like cells (GBM-SCs) to all-trans retinoic acid (RA). GBM-SCs were grown as non-adherent neurospheres in growth factor supplemented serum-free medium. RA treatment rapidly induced morphology changes, induced growth arrest at G1/G0 to S transition, decreased cyclin D1 expression and increased p27 expression. Immunofluorescence and western blot analysis indicated that RA induced the expression of lineage-specific differentiation markers Tuj1 and GFAP and reduced the expression of neural stem cell markers such as CD133, Msi-1, nestin and Sox-2. RA treatment dramatically decreased neurosphere-forming capacity, inhibited the ability of neurospheres to form colonies in soft agar and inhibited their capacity to propagate subcutaneous and intracranial xenografts. Expression microarray analysis identified ∼350 genes that were altered within 48 h of RA treatment. Affected pathways included retinoid signaling and metabolism, cell-cycle regulation, lineage determination, cell adhesion, cell-matrix interaction and cytoskeleton remodeling. Notch signaling was the most prominent of these RA-responsive pathways. Notch pathway downregulation was confirmed based on the downregulation of HES and HEY family members. Constitutive activation of Notch signaling with the Notch intracellular domain rescued GBM neurospheres from the RA-induced differentiation and stem cell depletion. Our findings identify mechanisms by which RA targets GBM-derived stem-like tumor-initiating cells and novel targets applicable to differentiation therapies for glioblastoma.

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ATRA inhibits proliferation of glioblastoma cells in vitro and in vivo, while promoting their differentiation.
“ATRA inhibits proliferation of glioblastoma cells in vitro and in vivo, while promoting their differentiation117,118.”
From Advances and challenges in retinoid delivery systems in regenerative and therapeutic medicine (2020) · cites this paper as [117]

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Abstract 5158: Differentiation of glioblastoma stem-like cells induced by retinoic acid
Ying, M., Sang, Y., Lal, B., Sun, P., Laterra, J., & Xia, S. (2010) · Cancer Research · doi:10.1158/1538-7445.am10-5158
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Authors: Ying, M., Wang, S., Sang, Y., Sun, P., Lal, B., Goodwin, C. R., Guerrero-Cazares, H., Quinones-Hinojosa, A., Laterra, J., & Xia, S.
Affiliations: Kennedy Krieger Institute (US)
Corresponding author: Xia, S
ORCID: Ying, M
Sang, Y
Sun, P
Lal, B
Goodwin, C R
Laterra, J
Xia, S
Venue: Oncogene
Publisher: Springer Science and Business Media LLC
Published: 2011-03-07
Volume: 30
Issue: 31
Pages: 3454-3467
ISSN: 0950-9232 (ISSN-L)
1476-5594
DOI: 10.1038/onc.2011.58
PMC: PMC3955956
OpenAlex: W2105823026
Cited by: 204
References: 55
Citations by year: 2026: 3 · 2025: 7 · 2024: 11 · 2023: 14 · 2022: 12 · 2021: 18 · 2020: 12 · 2019: 13 · 2018: 14 · 2017: 13 · 2016: 15 · 2015: 15 · 2014: 17 · 2013: 14 · 2012: 20
FWCI: 9.22
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Oncogene (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: Foundation for the National Institutes of Health
Howard Hughes Medical Institute
James S. McDonnell Foundation
National Institute of Neurological Disorders and Stroke (R01NS043987)
Topics: Health Sciences › Medicine › Genetics › Glioma Diagnosis and Treatment
Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords: glioblastoma stem cells, all-trans retinoic acid, Notch signaling, cancer stem cell differentiation, neurospheres, cyclin D1, p27, Notch intracellular domain, cancer stem cells, retinoid signaling, cell cycle arrest
MeSH terms: AC133 Antigen, Animals, Antineoplastic Agents, Brain Neoplasms, Cell Differentiation, Female, Glial Fibrillary Acidic Protein, Glioblastoma, Glycoproteins, Humans, Intermediate Filament Proteins, Mice, Nude, Nerve Tissue Proteins, Peptides, Tretinoin, Tubulin, Neoplastic Stem Cells, Antigens, CD, Gene Expression Regulation, Neoplastic, RNA-Binding Proteins, Proliferating Cell Nuclear Antigen, Cyclin D1, Gene Expression Profiling, Cell Line, Tumor, Mice, Receptors, Notch, SOXB1 Transcription Factors, Nestin

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Regulation of glioblastoma stem cells by retinoic acid: role for Notch pathway inhibition

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