Cisplatin Induces a Mitochondrial-ROS Response That Contributes to Cytotoxicity Depending on Mitochondrial Redox Status and Bioenergetic Functions
Cisplatin is one of the most effective and widely used anticancer agents for the treatment of several types of tumors. The cytotoxic effect of cisplatin is thought to be mediated primarily by the generation of nuclear DNA adducts, which, if not repaired, cause cell death as a consequence of DNA repl...
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| Published in | PloS one Vol. 8; no. 11; p. e81162 |
|---|---|
| Main Authors | , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
19.11.2013
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1932-6203 1932-6203 |
| DOI | 10.1371/journal.pone.0081162 |
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| Abstract | Cisplatin is one of the most effective and widely used anticancer agents for the treatment of several types of tumors. The cytotoxic effect of cisplatin is thought to be mediated primarily by the generation of nuclear DNA adducts, which, if not repaired, cause cell death as a consequence of DNA replication and transcription blockage. However, the ability of cisplatin to induce nuclear DNA (nDNA) damage per se is not sufficient to explain its high degree of effectiveness nor the toxic effects exerted on normal, post-mitotic tissues. Oxidative damage has been observed in vivo following exposure to cisplatin in several tissues, suggesting a role for oxidative stress in the pathogenesis of cisplatin-induced dose-limiting toxicities. However, the mechanism of cisplatin-induced generation of ROS and their contribution to cisplatin cytotoxicity in normal and cancer cells is still poorly understood. By employing a panel of normal and cancer cell lines and the budding yeast Saccharomyces cerevisiae as model system, we show that exposure to cisplatin induces a mitochondrial-dependent ROS response that significantly enhances the cytotoxic effect caused by nDNA damage. ROS generation is independent of the amount of cisplatin-induced nDNA damage and occurs in mitochondria as a consequence of protein synthesis impairment. The contribution of cisplatin-induced mitochondrial dysfunction in determining its cytotoxic effect varies among cells and depends on mitochondrial redox status, mitochondrial DNA integrity and bioenergetic function. Thus, by manipulating these cellular parameters, we were able to enhance cisplatin cytotoxicity in cancer cells. This study provides a new mechanistic insight into cisplatin-induced cell killing and may lead to the design of novel therapeutic strategies to improve anticancer drug efficacy. |
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| AbstractList | Cisplatin is one of the most effective and widely used anticancer agents for the treatment of several types of tumors. The cytotoxic effect of cisplatin is thought to be mediated primarily by the generation of nuclear DNA adducts, which, if not repaired, cause cell death as a consequence of DNA replication and transcription blockage. However, the ability of cisplatin to induce nuclear DNA (nDNA) damage per se is not sufficient to explain its high degree of effectiveness nor the toxic effects exerted on normal, post-mitotic tissues. Oxidative damage has been observed in vivo following exposure to cisplatin in several tissues, suggesting a role for oxidative stress in the pathogenesis of cisplatin-induced dose-limiting toxicities. However, the mechanism of cisplatin-induced generation of ROS and their contribution to cisplatin cytotoxicity in normal and cancer cells is still poorly understood. By employing a panel of normal and cancer cell lines and the budding yeast Saccharomyces cerevisiae as model system, we show that exposure to cisplatin induces a mitochondrial-dependent ROS response that significantly enhances the cytotoxic effect caused by nDNA damage. ROS generation is independent of the amount of cisplatin-induced nDNA damage and occurs in mitochondria as a consequence of protein synthesis impairment. The contribution of cisplatin-induced mitochondrial dysfunction in determining its cytotoxic effect varies among cells and depends on mitochondrial redox status, mitochondrial DNA integrity and bioenergetic function. Thus, by manipulating these cellular parameters, we were able to enhance cisplatin cytotoxicity in cancer cells. This study provides a new mechanistic insight into cisplatin-induced cell killing and may lead to the design of novel therapeutic strategies to improve anticancer drug efficacy. Cisplatin is one of the most effective and widely used anticancer agents for the treatment of several types of tumors. The cytotoxic effect of cisplatin is thought to be mediated primarily by the generation of nuclear DNA adducts, which, if not repaired, cause cell death as a consequence of DNA replication and transcription blockage. However, the ability of cisplatin to induce nuclear DNA (nDNA) damage per se is not sufficient to explain its high degree of effectiveness nor the toxic effects exerted on normal, post-mitotic tissues. Oxidative damage has been observed in vivo following exposure to cisplatin in several tissues, suggesting a role for oxidative stress in the pathogenesis of cisplatin-induced dose-limiting toxicities. However, the mechanism of cisplatin-induced generation of ROS and their contribution to cisplatin cytotoxicity in normal and cancer cells is still poorly understood. By employing a panel of normal and cancer cell lines and the budding yeast Saccharomyces cerevisiae as model system, we show that exposure to cisplatin induces a mitochondrial-dependent ROS response that significantly enhances the cytotoxic effect caused by nDNA damage. ROS generation is independent of the amount of cisplatin-induced nDNA damage and occurs in mitochondria as a consequence of protein synthesis impairment. The contribution of cisplatin-induced mitochondrial dysfunction in determining its cytotoxic effect varies among cells and depends on mitochondrial redox status, mitochondrial DNA integrity and bioenergetic function. Thus, by manipulating these cellular parameters, we were able to enhance cisplatin cytotoxicity in cancer cells. This study provides a new mechanistic insight into cisplatin-induced cell killing and may lead to the design of novel therapeutic strategies to improve anticancer drug efficacy.Cisplatin is one of the most effective and widely used anticancer agents for the treatment of several types of tumors. The cytotoxic effect of cisplatin is thought to be mediated primarily by the generation of nuclear DNA adducts, which, if not repaired, cause cell death as a consequence of DNA replication and transcription blockage. However, the ability of cisplatin to induce nuclear DNA (nDNA) damage per se is not sufficient to explain its high degree of effectiveness nor the toxic effects exerted on normal, post-mitotic tissues. Oxidative damage has been observed in vivo following exposure to cisplatin in several tissues, suggesting a role for oxidative stress in the pathogenesis of cisplatin-induced dose-limiting toxicities. However, the mechanism of cisplatin-induced generation of ROS and their contribution to cisplatin cytotoxicity in normal and cancer cells is still poorly understood. By employing a panel of normal and cancer cell lines and the budding yeast Saccharomyces cerevisiae as model system, we show that exposure to cisplatin induces a mitochondrial-dependent ROS response that significantly enhances the cytotoxic effect caused by nDNA damage. ROS generation is independent of the amount of cisplatin-induced nDNA damage and occurs in mitochondria as a consequence of protein synthesis impairment. The contribution of cisplatin-induced mitochondrial dysfunction in determining its cytotoxic effect varies among cells and depends on mitochondrial redox status, mitochondrial DNA integrity and bioenergetic function. Thus, by manipulating these cellular parameters, we were able to enhance cisplatin cytotoxicity in cancer cells. This study provides a new mechanistic insight into cisplatin-induced cell killing and may lead to the design of novel therapeutic strategies to improve anticancer drug efficacy. Cisplatin is one of the most effective and widely used anticancer agents for the treatment of several types of tumors. The cytotoxic effect of cisplatin is thought to be mediated primarily by the generation of nuclear DNA adducts, which, if not repaired, cause cell death as a consequence of DNA replication and transcription blockage. However, the ability of cisplatin to induce nuclear DNA (nDNA) damage per se is not sufficient to explain its high degree of effectiveness nor the toxic effects exerted on normal, post-mitotic tissues. Oxidative damage has been observed in vivo following exposure to cisplatin in several tissues, suggesting a role for oxidative stress in the pathogenesis of cisplatin-induced dose-limiting toxicities. However, the mechanism of cisplatin-induced generation of ROS and their contribution to cisplatin cytotoxicity in normal and cancer cells is still poorly understood. By employing a panel of normal and cancer cell lines and the budding yeast Saccharomyces cerevisiae as model system, we show that exposure to cisplatin induces a mitochondrial-dependent ROS response that significantly enhances the cytotoxic effect caused by nDNA damage. ROS generation is independent of the amount of cisplatin-induced nDNA damage and occurs in mitochondria as a consequence of protein synthesis impairment. The contribution of cisplatin-induced mitochondrial dysfunction in determining its cytotoxic effect varies among cells and depends on mitochondrial redox status, mitochondrial DNA integrity and bioenergetic function. Thus, by manipulating these cellular parameters, we were able to enhance cisplatin cytotoxicity in cancer cells. This study provides a new mechanistic insight into cisplatin-induced cell killing and may lead to the design of novel therapeutic strategies to improve anticancer drug efficacy. |
| Audience | Academic |
| Author | Ramalingam, Suresh S. Marullo, Rossella Doetsch, Paul W. Werner, Erica Moore, Bryn Altavilla, Giuseppe Degtyareva, Natalya |
| AuthorAffiliation | 1 Department of Hematology and Medical Oncology, Emory University, Atlanta, Georgia, United States of America 2 Department of Medical Oncology, University of Messina, Messina, Italy University of Pittsburgh, United States of America 4 Geisiner Medical Center, Danville, Pennsylvania, United States of America 5 Department of Radiation Oncology, Emory University, Atlanta, Georgia, United States of America 3 Department of Biochemistry, Emory University, Atlanta, Georgia, United States of America |
| AuthorAffiliation_xml | – name: 3 Department of Biochemistry, Emory University, Atlanta, Georgia, United States of America – name: 4 Geisiner Medical Center, Danville, Pennsylvania, United States of America – name: 5 Department of Radiation Oncology, Emory University, Atlanta, Georgia, United States of America – name: 1 Department of Hematology and Medical Oncology, Emory University, Atlanta, Georgia, United States of America – name: University of Pittsburgh, United States of America – name: 2 Department of Medical Oncology, University of Messina, Messina, Italy |
| Author_xml | – sequence: 1 givenname: Rossella surname: Marullo fullname: Marullo, Rossella – sequence: 2 givenname: Erica surname: Werner fullname: Werner, Erica – sequence: 3 givenname: Natalya surname: Degtyareva fullname: Degtyareva, Natalya – sequence: 4 givenname: Bryn surname: Moore fullname: Moore, Bryn – sequence: 5 givenname: Giuseppe surname: Altavilla fullname: Altavilla, Giuseppe – sequence: 6 givenname: Suresh S. surname: Ramalingam fullname: Ramalingam, Suresh S. – sequence: 7 givenname: Paul W. surname: Doetsch fullname: Doetsch, Paul W. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24260552$$D View this record in MEDLINE/PubMed |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Conceived and designed the experiments: RM EW ND PWD BM. Performed the experiments: RM. Analyzed the data: RM EW ND PWD SSR GA. Wrote the manuscript: RM EW ND PWD SSR GA. Competing Interests: The authors have declared that no competing interests exist. |
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| Snippet | Cisplatin is one of the most effective and widely used anticancer agents for the treatment of several types of tumors. The cytotoxic effect of cisplatin is... |
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| SubjectTerms | Adducts Animals Anticancer properties Antineoplastic Agents - pharmacology Antitumor agents Apoptosis Apoptosis - drug effects Baking yeast Biochemistry Biocompatibility Blockage Cancer Cancer research Cancer treatment Cell death Cell Line, Tumor Cell Nucleus - drug effects Cell Nucleus - metabolism Chemotherapy Cisplatin Cisplatin - pharmacology Cytotoxicity Damage Deoxyribonucleic acid DNA DNA - chemistry DNA - metabolism DNA adducts DNA Adducts - chemistry DNA biosynthesis DNA Damage DNA Repair - drug effects DNA replication Drug development Drug dosages Drug efficacy Exposure Hematology Humans Kinases Medical prognosis Medical research Mice Mitochondria Mitochondria - drug effects Mitochondria - metabolism Mitochondrial DNA Oncology Oxidation-Reduction Oxidative stress Pathogenesis Phosphorylation Protein biosynthesis Protein synthesis Reactive Oxygen Species - agonists Reactive Oxygen Species - metabolism Saccharomyces cerevisiae Saccharomyces cerevisiae - drug effects Saccharomyces cerevisiae - genetics Saccharomyces cerevisiae - metabolism Signal transduction Stress response Studies Survival analysis Tissues Toxicity Transcription Transcription (Genetics) Tumor cell lines Tumors Yeast |
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| Title | Cisplatin Induces a Mitochondrial-ROS Response That Contributes to Cytotoxicity Depending on Mitochondrial Redox Status and Bioenergetic Functions |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/24260552 https://www.proquest.com/docview/1465947735 https://www.proquest.com/docview/1461884990 https://pubmed.ncbi.nlm.nih.gov/PMC3834214 https://doaj.org/article/6f0797757513416b837bd2907dacf006 http://dx.doi.org/10.1371/journal.pone.0081162 |
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