HIF-2α maintains an undifferentiated state in neural crest-like human neuroblastoma tumor-initiating cells

Pietras, Alexander; Hansford, Loen M.; Johnsson, A. Sofie; Bridges, Esther; Sjölund, Jonas; Gisselsson, David; Rehn, Matilda; Beckman, Siv; Noguera, Rosa; Navarro, Samuel; Cammenga, Jörg; Fredlund, Erik; Kaplan, David R.; Påhlman, Sven

doi:10.1073/pnas.0904606106

Cited by 135Neuroblastoma Research and TreatmentsCancer, Hypoxia, and MetabolismAngiogenesis and VEGF in Cancer

HIF-2α maintains an undifferentiated state in neural crest-like human neuroblastoma tumor-initiating cells

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Pietras, Alexander, Hansford, Loen M., Johnsson, A. Sofie, Bridges, Esther, Sjölund, Jonas, Gisselsson, David, Rehn, Matilda, Beckman, Siv +6 more·2009·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.0904606106PMC PMC2745331

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Abstract

High hypoxia-inducible factor-2α (HIF-2α) protein levels predict poor outcome in neuroblastoma, and hypoxia dedifferentiates cultured neuroblastoma cells toward a neural crest-like phenotype. Here, we identify HIF-2α as a marker of normoxic neural crest-like neuroblastoma tumor-initiating/stem cells (TICs) isolated from patient bone marrows. Knockdown of HIF-2α reduced VEGF expression and induced partial sympathetic neuronal differentiation when these TICs were grown in vitro under stem cell-promoting conditions. Xenograft tumors of HIF-2α-silenced cells were widely necrotic, poorly vascularized, and resembled the bulk of tumor cells in clinical neuroblastomas by expressing additional sympathetic neuronal markers, whereas control tumors were immature, well-vascularized, and stroma-rich. Thus, HIF-2α maintains an undifferentiated state of neuroblastoma TICs. Because low differentiation is associated with poor outcome and angiogenesis is crucial for tumor growth, HIF-2α is an attractive target for neuroblastoma therapy.

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HIF-2α knockdown in glioblastoma and neuroblastoma results in poorly vascularized tumors.
“HIF-2α knockdown in glioblastoma and neuroblastoma results in poorly vascularized tumors (Li et al., 2009;Pietras et al., 2009).”
From Therapeutic targeting of hypoxia and hypoxia-inducible factors in cancer (2016) · cites this paper as Pietras et al., 2009

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Hypoxia-Inducible Factors in Tumor Cell Differentiation and Tumor Vascularization
Pietras, A. (2010) · Lund University Publications (Lund University)
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Hypoxia alters gene expression in human neuroblastoma cells toward an immature and neural crest-like phenotype
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High levels of HIF‐2α highlight an immature neural crest‐like neuroblastoma cell cohort located in a perivascular niche
Pietras, A., Gisselsson, D., Øra, I., Noguera, R., Beckman, S., Navarro, S., & Påhlman, S. (2008) · The Journal of Pathology · doi:10.1002/path.2304 · Cited by 116 · see citing works
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Authors: Pietras, A., Hansford, L. M., Johnsson, A. S., Bridges, E., Sjölund, J., Gisselsson, D., Rehn, M., Beckman, S., Noguera, R., Navarro, S., Cammenga, J., Fredlund, E., Kaplan, D. R., & Påhlman, S.
Affiliations: Lund University (SE)
University of Toronto (CA)
Departments of cClinical Genetics and
Universitat de València (ES)
ORCID: Pietras, Alexander
Bridges, Esther
Sjölund, Jonas
Gisselsson, David
Rehn, Matilda
Noguera, Rosa
Navarro, Samuel
Cammenga, Jörg
Kaplan, David R.
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2009-09-29
Volume: 106
Issue: 39
Pages: 16805-16810
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.0904606106
PMC: PMC2745331
OpenAlex: W1967063990
Cited by: 135
References: 32
Citations by year: 2026: 1 · 2025: 2 · 2024: 2 · 2023: 4 · 2022: 5 · 2021: 6 · 2020: 10 · 2019: 5 · 2018: 11 · 2017: 13 · 2016: 9 · 2015: 8 · 2014: 11 · 2013: 10 · 2012: 14
FWCI: 8.11
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Lund University Publications (Lund University) (submittedVersion)
Topics: Health Sciences › Medicine › Neurology › Neuroblastoma Research and Treatments
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
Keywords: HIF-2α, neuroblastoma, cancer stem cells, neural crest-like cells, hypoxia, neuronal differentiation, vascular endothelial growth factor, tumor angiogenesis, tumor necrosis, bone marrow, stem cell niche, therapeutic target
MeSH terms: Endothelial PAS Domain-Containing Protein 1, Animals, Cell Differentiation, Female, Humans, Mice, Nude, Neural Crest, Neuroblastoma, Down-Regulation, Cell Hypoxia, Vascular Endothelial Growth Factors, Cell Line, Tumor, Mice, Basic Helix-Loop-Helix Proteins, Basic Helix-Loop-Helix Transcription Factors

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HIF-2α maintains an undifferentiated state in neural crest-like human neuroblastoma tumor-initiating cells

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