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The Oncogene HER2/neu (ERBB2) Requires the Hypoxia-inducible Factor HIF-1 for Mammary Tumor Growth and Anoikis Resistance
Journal article   Open access   Peer reviewed

The Oncogene HER2/neu (ERBB2) Requires the Hypoxia-inducible Factor HIF-1 for Mammary Tumor Growth and Anoikis Resistance

Kelly A Whelan, Luciana P Schwab, Sergey V Karakashev, Lisa Franchetti, Gregg J Johannes, Tiffany N Seagroves and Mauricio J Reginato
The Journal of biological chemistry, v 288(22), pp 15865-15877
31 May 2013
PMID: 23585570
url
https://doi.org/10.1074/jbc.M112.426999View
Published, Version of Record (VoR) Open

Abstract

Molecular Bases of Disease HIF-1 Epidermal Growth Factor Receptor (EGFR) ERBB2 Cell Signaling Anoikis Breast Cancer Hypoxia Inducible Factor Apoptosis Three-dimensional Culture
Background: Oncogene HER2 (ERBB2) regulates breast cancer growth and anoikis resistance. Results: ERBB2 requires hypoxia-inducible factor (HIF)-1 for breast cancer growth in vivo and anoikis resistance in vitro . Conclusion: HIF-1 plays a critical role in ERBB2-positive breast cancers. Significance: Genes co-regulated by ERBB2 and HIF-1 may be novel therapeutic targets for treating breast cancer. ERBB2, a receptor tyrosine kinase amplified in breast cancer, is a well established regulator of tumor growth in vivo and anoikis resistance leading to disruption of architecture in three-dimensional mammary epithelial acinar structures in vitro . ERBB2 promotes anoikis resistance by maintaining signaling pathways and by rescuing metabolic defects and thus inhibiting accumulation of deleterious reactive oxygen species. Recent evidence suggests that hypoxia, via hypoxia-inducible factors (HIFs), can inhibit anoikis; thus, we hypothesized that HIF-1 may play a role in ERBB2-mediated anoikis resistance and oncogenesis. Indeed, tumors isolated from MMTV-Neu mice contain elevated HIF-1α levels and tumor cells created from MMTV-Neu mice harboring deletion of Hif1 α alleles reduced primary tumor growth in vivo . ERBB2 overexpressing cancer cells stabilize HIF under normoxic conditions and require HIF-1 for ERBB2-mediated anchorage-independence, three-dimensional culture growth and anoikis resistance. HIF-1 reduction in ERBB2 cells was associated with induction of the pro-anoikis protein BIM and decreased ERK and AKT signaling during cell detachment. ERBB2-mediated inhibition of metabolic defects, including decreased reactive oxygen species generation in suspension, required HIF-1 expression that was critical for ERBB2-mediated oncogenesis. Gene expression profiling of hypoxic three-dimensional acinar structures identified a number of genes elevated in response to hypoxia that are known ERBB2 targets, suggesting that hypoxic conditions and ERBB2 overexpression share both phenotypic and genetic components via HIF-1 regulation. Thus, our data demonstrate that ERBB2 requires HIF-1 for tumor growth and suggest that HIF is a major downstream regulator of ERBB2 that protects cells from anoikis and metabolic stress caused by decreased matrix adhesion.

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Collaboration types
Domestic collaboration
Web of Science research areas
Biochemistry & Molecular Biology
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