Cited by 187Cancer, Hypoxia, and MetabolismAmino Acid Enzymes and MetabolismCancer, Lipids, and Metabolism

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Targeting Glutamine Metabolism in Breast Cancer with Aminooxyacetate

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Korangath, Preethi, Teo, Wei Wen, Sadik, Helen, Han, Liangfeng, Mori, Noriko, Huijts, Charlotte M., Wildes, Flonne, Bharti, Santosh, Zhang, Zhe, Santa-Maria, Cesar A., Tsai, Hualing, Dang, Chi V., Stearns, Vered, Bhujwalla, Zaver M., Sukumar, Saraswati·2015·Clinical Cancer Research

DOI 10.1158/1078-0432.ccr-14-1200PMC PMC4696069

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Abstract

Purpose: Glutamine addiction in c-MYC–overexpressing breast cancer is targeted by the aminotransferase inhibitor, aminooxyacetate (AOA). However, the mechanism of ensuing cell death remains unresolved. Experimental Design: A correlation between glutamine dependence for growth and c-MYC expression was studied in breast cancer cell lines. The cytotoxic effects of AOA, its correlation with high c-MYC expression, and effects on enzymes in the glutaminolytic pathway were investigated. AOA-induced cell death was assessed by measuring changes in metabolite levels by magnetic resonance spectroscopy (MRS), the effects of amino acid depletion on nucleotide synthesis by cell-cycle and bromodeoxyuridine (BrdUrd) uptake analysis, and activation of the endoplasmic reticulum (ER) stress–mediated pathway. Antitumor effects of AOA with or without common chemotherapies were determined in breast cancer xenografts in immunodeficient mice and in a transgenic MMTV-rTtA-TetO-myc mouse mammary tumor model. Results: We established a direct correlation between c-MYC overexpression, suppression of glutaminolysis, and AOA sensitivity in most breast cancer cells. MRS, cell-cycle analysis, and BrdUrd uptake measurements indicated depletion of aspartic acid and alanine leading to cell-cycle arrest at S-phase by AOA. Activation of components of the ER stress–mediated pathway, initiated through GRP78, led to apoptotic cell death. AOA inhibited growth of SUM159, SUM149, and MCF-7 xenografts and c-myc–overexpressing transgenic mouse mammary tumors. In MDA-MB-231, AOA was effective only in combination with chemotherapy. Conclusions: AOA mediates its cytotoxic effects largely through the stress response pathway. The preclinical data of AOA's effectiveness provide a strong rationale for further clinical development, particularly for c-MYC–overexpressing breast cancers. Clin Cancer Res; 21(14); 3263–73. ©2015 AACR.

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Authors: Korangath, P., Teo, W. W., Sadik, H., Han, L., Mori, N., Huijts, C. M., Wildes, F., Bharti, S., Zhang, Z., Santa-Maria, C. A., Tsai, H., Dang, C. V., Stearns, V., Bhujwalla, Z. M., & Sukumar, S.
Affiliations: Johns Hopkins University (US)
2Department of Radiology, Johns Hopkins University School of Medicine, Baltimore, Maryland.
1Department of Oncology, Johns Hopkins University School of Medicine, Baltimore, Maryland.
University of Pennsylvania (US)
Corresponding author: Sukumar, Saraswati
ORCID: Korangath, Preethi
Teo, Wei Wen
Bharti, Santosh
Zhang, Zhe
Santa-Maria, Cesar A.
Dang, Chi V.
Stearns, Vered
Bhujwalla, Zaver M.
Sukumar, Saraswati
Venue: Clinical Cancer Research
Publisher: American Association for Cancer Research (AACR)
Published: 2015-07-14
Volume: 21
Issue: 14
Pages: 3263-3273
ISSN: 1078-0432 (ISSN-L)
1557-3265
DOI: 10.1158/1078-0432.ccr-14-1200
PMC: PMC4696069
OpenAlex: W2011628468
Cited by: 182
References: 40
Citations by year: 2026: 11 · 2025: 11 · 2024: 18 · 2023: 7 · 2022: 30 · 2021: 15 · 2020: 28 · 2019: 13 · 2018: 13 · 2017: 17 · 2016: 15 · 2015: 3
FWCI: 5.29
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Clinical Cancer Research (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: University of Pennsylvania
National Cancer Institute (R01CA051497, P30CA060553, P30CA006973, P30CA016520)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Amino Acid Enzymes and Metabolism
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Lipids, and Metabolism
Keywords: aminooxyacetic acid, glutamine metabolism, glutaminolysis, MYC overexpression, breast cancer, endoplasmic reticulum stress, GRP78, apoptosis, S phase arrest, amino acid starvation, nucleotide synthesis, combination chemotherapy, xenografts
MeSH terms: Endoplasmic Reticulum Chaperone BiP, Aminooxyacetic Acid, Animals, Antineoplastic Agents, Breast Neoplasms, Enzyme Inhibitors, Female, Glutamine, Humans, Mice, Transgenic, Magnetic Resonance Spectroscopy, Xenograft Model Antitumor Assays, Cell Line, Tumor, Mice

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Targeting Glutamine Metabolism in Breast Cancer with Aminooxyacetate

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