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Dual Oxidase-Induced Sustained Generation of Hydrogen Peroxide Contributes to Pharmacologic Ascorbate-Induced Cytotoxicity
Journal article   Open access   Peer reviewed

Dual Oxidase-Induced Sustained Generation of Hydrogen Peroxide Contributes to Pharmacologic Ascorbate-Induced Cytotoxicity

Adrienne R Gibson, Brianne R O'Leary, Juan Du, Ehab H Sarsour, Amanda L Kalen, Brett A Wagner, Jeffrey M Stolwijk, Kelly C Falls-Hubert, Matthew S Alexander, Rory S Carroll, …
Cancer research (Chicago, Ill.), Vol.80(7), pp.1401-1413
04/01/2020
DOI: 10.1158/0008-5472.CAN-19-3094
PMCID: PMC7127976
PMID: 32041838
url
https://doi.org/10.1158/0008-5472.CAN-19-3094View
Published (Version of record) Open Access

Abstract

Pharmacologic ascorbate treatment (P-AscH , high-dose, intravenous vitamin C) results in a transient short-term increase in the flux of hydrogen peroxide that is preferentially cytotoxic to cancer cells versus normal cells. This study examines whether an increase in hydrogen peroxide is sustained posttreatment and potential mechanisms involved in this process. Cellular bioenergetic profiling following treatment with P-AscH was examined in tumorigenic and nontumorigenic cells. P-AscH resulted in sustained increases in the rate of cellular oxygen consumption (OCR) and reactive oxygen species (ROS) in tumor cells, with no changes in nontumorigenic cells. Sources for this increase in ROS and OCR were DUOX 1 and 2, which are silenced in pancreatic ductal adenocarcinoma, but upregulated with P-AscH treatment. An inducible catalase system, to test causality for the role of hydrogen peroxide, reversed the P-AscH -induced increases in DUOX, whereas DUOX inhibition partially rescued P-AscH -induced toxicity. In addition, DUOX was significantly downregulated in pancreatic cancer specimens compared with normal pancreas tissues. Together, these results suggest that P-AscH -induced toxicity may be enhanced by late metabolic shifts in tumor cells, resulting in a feed-forward mechanism for generation of hydrogen peroxide and induction of metabolic stress through enhanced DUOX expression and rate of oxygen consumption. SIGNIFICANCE: A high dose of vitamin C, in addition to delivering an acute exposure of H O to tumor cells, activates DUOX in pancreatic cancer cells, which provide sustained production of H O .
Administration, Intravenous Animals Ascorbic Acid - pharmacology Ascorbic Acid - therapeutic use Carcinoma, Pancreatic Ductal - genetics Carcinoma, Pancreatic Ductal - pathology Carcinoma, Pancreatic Ductal - therapy Cell Line, Tumor Chemotherapy, Adjuvant - methods Dose-Response Relationship, Drug Down-Regulation - genetics Dual Oxidases - genetics Dual Oxidases - metabolism Gene Expression Regulation, Neoplastic - drug effects Humans Hydrogen Peroxide - metabolism Mice Oxidative Stress - drug effects Oxygen - metabolism Oxygen Consumption - drug effects Pancreas - pathology Pancreatic Neoplasms - genetics Pancreatic Neoplasms - pathology Pancreatic Neoplasms - therapy Pancreaticoduodenectomy Reactive Oxygen Species - metabolism Up-Regulation - drug effects Xenograft Model Antitumor Assays

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