U.S. Department of EnergyOffice of Scientific and Technical Information
Oxidative phosphorylation-dependent regulation of cancer cell apoptosis in response to anticancer agents
Abstract
Cancer cells tend to develop resistance to various types of anticancer agents, whether they adopt similar or distinct mechanisms to evade cell death in response to a broad spectrum of cancer therapeutics is not fully defined. Current study concludes that DNA-damaging agents (etoposide and doxorubicin), ER stressor (thapsigargin), and histone deacetylase inhibitor (apicidin) target oxidative phosphorylation (OXPHOS) for apoptosis induction, whereas other anticancer agents including staurosporine, taxol, and sorafenib induce apoptosis in an OXPHOS-independent manner. DNA-damaging agents promoted mitochondrial biogenesis accompanied by increased accumulation of cellular and mitochondrial ROS, mitochondrial protein-folding machinery, and mitochondrial unfolded protein response. Induction of mitochondrial biogenesis occurred in a caspase activation-independent mechanism but was reduced by autophagy inhibition and p53-deficiency. Abrogation of complex-I blocked DNA-damage-induced caspase activation and apoptosis, whereas inhibition of complex-II or a combined deficiency of OXPHOS complexes I, III, IV, and V due to impaired mitochondrial protein synthesis did not modulate caspase activity. Mechanistic analysis revealed that inhibition of caspase activation in response to anticancer agents associates with decreased release of mitochondrial cytochrome c in complex-I-deficient cells compared with wild type (WT) cells. Gross OXPHOS deficiencies promoted increased release of apoptosis-inducing factor from mitochondria compared with WT or complex-I-deficient cells, suggesting thatmore »
- Authors:
-
[1]
- Roswell Park Cancer Institute, Buffalo, NY (United States)
- Univ. of Arkansas, Fayetteville, AR (United States)
- Pioneer Valley Life Sciences Inst., Springfield, MA (United States)
- Publication Date:
- Research Org.:
- Roswell Park Cancer Institute, Buffalo, NY (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1239287
- Grant/Contract Number:
- FG02-01ER15161
- Resource Type:
- Journal Article: Accepted Manuscript
- Journal Name:
- Cell Death and Disease
- Additional Journal Information:
- Journal Volume: 6; Journal Issue: 11; Journal ID: ISSN 2041-4889
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Yadav, N., Kumar, S., Marlowe, T., Chaudhary, A. K., Kumar, R., Wang, J., O'Malley, J., Boland, P. M., Jayanthi, S., Kumar, T. K. S., Yadava, N., and Chandra, D. Oxidative phosphorylation-dependent regulation of cancer cell apoptosis in response to anticancer agents. United States: N. p., 2015.
Web. doi:10.1038/cddis.2015.305.
Yadav, N., Kumar, S., Marlowe, T., Chaudhary, A. K., Kumar, R., Wang, J., O'Malley, J., Boland, P. M., Jayanthi, S., Kumar, T. K. S., Yadava, N., & Chandra, D. Oxidative phosphorylation-dependent regulation of cancer cell apoptosis in response to anticancer agents. United States. https://doi.org/10.1038/cddis.2015.305
Yadav, N., Kumar, S., Marlowe, T., Chaudhary, A. K., Kumar, R., Wang, J., O'Malley, J., Boland, P. M., Jayanthi, S., Kumar, T. K. S., Yadava, N., and Chandra, D. 2015.
"Oxidative phosphorylation-dependent regulation of cancer cell apoptosis in response to anticancer agents". United States. https://doi.org/10.1038/cddis.2015.305. https://www.osti.gov/servlets/purl/1239287.
@article{osti_1239287,
title = {Oxidative phosphorylation-dependent regulation of cancer cell apoptosis in response to anticancer agents},
author = {Yadav, N. and Kumar, S. and Marlowe, T. and Chaudhary, A. K. and Kumar, R. and Wang, J. and O'Malley, J. and Boland, P. M. and Jayanthi, S. and Kumar, T. K. S. and Yadava, N. and Chandra, D.},
abstractNote = {Cancer cells tend to develop resistance to various types of anticancer agents, whether they adopt similar or distinct mechanisms to evade cell death in response to a broad spectrum of cancer therapeutics is not fully defined. Current study concludes that DNA-damaging agents (etoposide and doxorubicin), ER stressor (thapsigargin), and histone deacetylase inhibitor (apicidin) target oxidative phosphorylation (OXPHOS) for apoptosis induction, whereas other anticancer agents including staurosporine, taxol, and sorafenib induce apoptosis in an OXPHOS-independent manner. DNA-damaging agents promoted mitochondrial biogenesis accompanied by increased accumulation of cellular and mitochondrial ROS, mitochondrial protein-folding machinery, and mitochondrial unfolded protein response. Induction of mitochondrial biogenesis occurred in a caspase activation-independent mechanism but was reduced by autophagy inhibition and p53-deficiency. Abrogation of complex-I blocked DNA-damage-induced caspase activation and apoptosis, whereas inhibition of complex-II or a combined deficiency of OXPHOS complexes I, III, IV, and V due to impaired mitochondrial protein synthesis did not modulate caspase activity. Mechanistic analysis revealed that inhibition of caspase activation in response to anticancer agents associates with decreased release of mitochondrial cytochrome c in complex-I-deficient cells compared with wild type (WT) cells. Gross OXPHOS deficiencies promoted increased release of apoptosis-inducing factor from mitochondria compared with WT or complex-I-deficient cells, suggesting that cells harboring defective OXPHOS trigger caspase-dependent as well as caspase-independent apoptosis in response to anticancer agents. Interestingly, DNA-damaging agent doxorubicin showed strong binding to mitochondria, which was disrupted by complex-I-deficiency but not by complex-II-deficiency. Thapsigargin-induced caspase activation was reduced upon abrogation of complex-I or gross OXPHOS deficiency whereas a reverse trend was observed with apicidin. Together, these finding provide a new strategy for differential mitochondrial targeting in cancer therapy.},
doi = {10.1038/cddis.2015.305},
url = {https://www.osti.gov/biblio/1239287},
journal = {Cell Death and Disease},
issn = {2041-4889},
number = 11,
volume = 6,
place = {United States},
year = {Thu Nov 05 00:00:00 EST 2015},
month = {Thu Nov 05 00:00:00 EST 2015}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 85 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Hallmarks of Cancer: The Next Generation
journal, March 2011
- Hanahan, Douglas; Weinberg, Robert A.
- Cell, Vol. 144, Issue 5
Mitochondrial and postmitochondrial survival signaling in cancer
journal, May 2014
- Yadav, Neelu; Chandra, Dhyan
- Mitochondrion, Vol. 16
Defects in mitochondrial metabolism and cancer
journal, July 2014
- Gaude, Edoardo; Frezza, Christian
- Cancer & Metabolism, Vol. 2, Issue 1
Selective anticancer strategies via intervention of the death pathways relevant to cell transformation
journal, April 2008
- Li, Q-X; Yu, D. H.; Liu, G.
- Cell Death & Differentiation, Vol. 15, Issue 8
Mitochondria as Therapeutic Targets for the Treatment of Malignant Disease
journal, December 2011
- Fulda, Simone; Kroemer, Guido
- Antioxidants & Redox Signaling, Vol. 15, Issue 12
Mitochondria: gatekeepers of response to chemotherapy
journal, December 2013
- Sarosiek, Kristopher A.; Ni Chonghaile, Triona; Letai, Anthony
- Trends in Cell Biology, Vol. 23, Issue 12
ABT-199, a potent and selective BCL-2 inhibitor, achieves antitumor activity while sparing platelets
journal, January 2013
- Souers, Andrew J.; Leverson, Joel D.; Boghaert, Erwin R.
- Nature Medicine, Vol. 19, Issue 2
ABT-199: Taking Dead Aim at BCL-2
journal, February 2013
- Davids, Matthew S.; Letai, Anthony
- Cancer Cell, Vol. 23, Issue 2
Lack of Oxidative Phosphorylation and Low Mitochondrial Membrane Potential Decrease Susceptibility to Apoptosis and Do Not Modulate the Protective Effect of Bcl-x L in Osteosarcoma Cells
journal, March 2000
- Dey, Runu; Moraes, Carlos T.
- Journal of Biological Chemistry, Vol. 275, Issue 10
Genetic insights into OXPHOS defect and its role in cancer
journal, June 2011
- Chandra, Dhyan; Singh, Keshav K.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1807, Issue 6
Mitochondria and cancer
journal, September 2012
- Wallace, Douglas C.
- Nature Reviews Cancer, Vol. 12, Issue 10
Mitochondrially Localized Active Caspase-9 and Caspase-3 Result Mostly from Translocation from the Cytosol and Partly from Caspase-mediated Activation in the Organelle: LACK OF EVIDENCE FOR Apaf-1-MEDIATED PROCASPASE-9 ACTIVATION IN THE MITOCHONDRIA
journal, February 2003
- Chandra, Dhyan; Tang, Dean G.
- Journal of Biological Chemistry, Vol. 278, Issue 19
Induction of a Caspase-3-like Activity by Calcium in Normal Cytosolic Extracts Triggers Nuclear Apoptosis in a Cell-free System
journal, July 1998
- Juin, Philippe; Pelletier, Maude; Oliver, Lisa
- Journal of Biological Chemistry, Vol. 273, Issue 28
Transformations of the macromolecular landscape at mitochondria during DNA-damage-induced apoptotic cell death
journal, October 2014
- Yadav, N.; Pliss, A.; Kuzmin, A.
- Cell Death & Disease, Vol. 5, Issue 10
Loss of p53 causes mitochondrial DNA depletion and altered mitochondrial reactive oxygen species homeostasis
journal, May 2009
- Lebedeva, Maria A.; Eaton, Jana S.; Shadel, Gerald S.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1787, Issue 5
BAX supports the mitochondrial network, promoting bioenergetics in nonapoptotic cells
journal, June 2011
- Boohaker, Rebecca J.; Zhang, Ge; Carlson, Adina Loosley
- American Journal of Physiology-Cell Physiology, Vol. 300, Issue 6
Human OXR1 maintains mitochondrial DNA integrity and counteracts hydrogen peroxide-induced oxidative stress by regulating antioxidant pathways involving p21
journal, December 2014
- Yang, Mingyi; Luna, Luisa; Sørbø, Jan Gunnar
- Free Radical Biology and Medicine, Vol. 77
TZDs reduce mitochondrial ROS production and enhance mitochondrial biogenesis
journal, January 2009
- Fujisawa, Kazuo; Nishikawa, Takeshi; Kukidome, Daisuke
- Biochemical and Biophysical Research Communications, Vol. 379, Issue 1
Human mitochondrial DNA deletions associated with mutations in the gene encoding Twinkle, a phage T7 gene 4-like protein localized in mitochondria
journal, July 2001
- Spelbrink, Johannes N.; Li, Fang-Yuan; Tiranti, Valeria
- Nature Genetics, Vol. 28, Issue 3
DNA Polymerase γ, The Mitochondrial Replicase
journal, June 2004
- Kaguni, Laurie S.
- Annual Review of Biochemistry, Vol. 73, Issue 1
ROS-mediated mechanisms of autophagy stimulation and their relevance in cancer therapy
journal, October 2010
- Dewaele, Michael; Maes, Hannelore; Agostinis, Patrizia
- Autophagy, Vol. 6, Issue 7
Regulation of the Intrinsic Apoptosis Pathway by Reactive Oxygen Species
journal, August 2013
- Wu, Chu-Chiao; Bratton, Shawn B.
- Antioxidants & Redox Signaling, Vol. 19, Issue 6
The NDUFA1 gene product (MWFE protein) is essential for activity of complex I in mammalian mitochondria
journal, April 1999
- Au, H. C.; Seo, B. B.; Matsuno-Yagi, A.
- Proceedings of the National Academy of Sciences, Vol. 96, Issue 8
Chinese hamster cell mutant with defective mitochondrial protein synthesis
journal, July 1977
- Ditta, G.; Soderberg, K.; Scheffler, I. E.
- Nature, Vol. 268, Issue 5615
Resveratrol depletes mitochondrial DNA and inhibition of autophagy enhances resveratrol-induced caspase activation
journal, September 2013
- Prabhu, Varun; Srivastava, Pragya; Yadav, Neelu
- Mitochondrion, Vol. 13, Issue 5
The selection of Chinese hamster cells deficient in oxidative energy metabolism
journal, July 1976
- Ditta, G.; Soderberg, K.; Landy, F.
- Somatic Cell Genetics, Vol. 2, Issue 4
4E-BP Extends Lifespan upon Dietary Restriction by Enhancing Mitochondrial Activity in Drosophila
journal, October 2009
- Zid, Brian M.; Rogers, Aric N.; Katewa, Subhash D.
- Cell, Vol. 139, Issue 1
Mitochondrial Cardiolipin Is Required for Nlrp3 Inflammasome Activation
journal, August 2013
- Iyer, Shankar S.; He, Qiong; Janczy, John R.
- Immunity, Vol. 39, Issue 2
Oxidized Mitochondrial DNA Activates the NLRP3 Inflammasome during Apoptosis
journal, March 2012
- Shimada, Kenichi; Crother, Timothy R.; Karlin, Justin
- Immunity, Vol. 36, Issue 3
Mitochondrial functions during cell death, a complex (I–V) dilemma
journal, May 2003
- Ricci, J-E; Waterhouse, N.; Green, D. R.
- Cell Death & Differentiation, Vol. 10, Issue 5
Composition and Dynamics of Human Mitochondrial Nucleoids
journal, April 2003
- Garrido, Nuria; Griparic, Lorena; Jokitalo, Eija
- Molecular Biology of the Cell, Vol. 14, Issue 4
p53 regulates mtDNA copy number and mitocheckpoint pathway
journal, January 2009
- Singh, KeshavK; Kulawiec, Mariola; Ayyasamy, Vanniarajan
- Journal of Carcinogenesis, Vol. 8, Issue 1
Novel role of p53 in maintaining mitochondrial genetic stability through interaction with DNA Pol γ
journal, September 2005
- Achanta, Geetha; Sasaki, Ryohei; Feng, Li
- The EMBO Journal, Vol. 24, Issue 19
The Mitochondrial Production of Reactive Oxygen Species: Mechanisms and Implications in Human Pathology
journal, September 2001
- Lenaz, Giorgio
- IUBMB Life (International Union of Biochemistry and Molecular Biology: Life), Vol. 52, Issue 3-5
Mitochondrial DNA determines the cellular response to cancer therapeutic agents
journal, November 1999
- Singh, Keshav K.; Russell, James; Sigala, Barbara
- Oncogene, Vol. 18, Issue 48
Etoposide Induces ATM-Dependent Mitochondrial Biogenesis through AMPK Activation
journal, April 2008
- Fu, Xuan; Wan, Shan; Lyu, Yi Lisa
- PLoS ONE, Vol. 3, Issue 4
Discrete mechanisms of mTOR and cell cycle regulation by AMPK agonists independent of AMPK
journal, January 2014
- Liu, X.; Chhipa, R. R.; Pooya, S.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 4
Investigations of the potential effects of phosphorylation of the MWFE and ESSS subunits on complex I activity and assembly
journal, January 2008
- Yadava, N.; Potluri, P.; Scheffler, I. E.
- The International Journal of Biochemistry & Cell Biology, Vol. 40, Issue 3
The role of the ESSS protein in the assembly of a functional and stable mammalian mitochondrial complex I (NADH-ubiquinone oxidoreductase): Mammalian cells with severe complex I deficiency
journal, July 2004
- Potluri, Prasanth; Yadava, Nagendra; Scheffler, Immo E.
- European Journal of Biochemistry, Vol. 271, Issue 15
DNA supercoiling suppresses real-time PCR: a new approach to the quantification of mitochondrial DNA damage and repair
journal, February 2007
- Chen, Jinsong; Kadlubar, Fred F.; Chen, Junjian Z.
- Nucleic Acids Research, Vol. 35, Issue 4
Real time quantitative PCR.
journal, October 1996
- Heid, C. A.; Stevens, J.; Livak, K. J.
- Genome Research, Vol. 6, Issue 10, p. 986-994
Decreased mitochondrial DNA content in blood samples of patients with stage I breast cancer
journal, December 2009
- Xia, Peng; An, Han-Xiang; Dang, Cheng-Xue
- BMC Cancer, Vol. 9, Issue 1
Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks
journal, March 2012
- Trapnell, Cole; Roberts, Adam; Goff, Loyal
- Nature Protocols, Vol. 7, Issue 3
Induction of regulatory T cells by macrophages is dependent on production of reactive oxygen species
journal, September 2010
- Kraaij, Marina D.; Savage, Nigel D. L.; van der Kooij, Sandra W.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 41
Mitochondrial reactive oxygen species promote production of proinflammatory cytokines and are elevated in TNFR1-associated periodic syndrome (TRAPS)
journal, January 2011
- Bulua, Ariel C.; Simon, Anna; Maddipati, Ravikanth
- The Journal of Experimental Medicine, Vol. 208, Issue 3
Bcl-2 and Mitochondrial Oxygen Radicals: NEW APPROACHES WITH REACTIVE OXYGEN SPECIES-SENSITIVE PROBES
journal, October 1999
- Esposti, Mauro Degli; Hatzinisiriou, Irene; McLennan, Holly
- Journal of Biological Chemistry, Vol. 274, Issue 42
Precision medicine in acute lymphoblastic leukemia
journal, October 2020
- Pui, Ching-Hon
- Frontiers of Medicine, Vol. 14, Issue 6
Staging the Tumor and Staging the Host: Pretreatment Combined Neutrophil Lymphocyte Ratio and Modified Glasgow Prognostic Score Is Associated with Overall Survival in Patients with Esophagogastric Cancers Undergoing Treatment with Curative Intent
journal, September 2020
- McSorley, Stephen T.; Lau, Hiu Y. N.; McIntosh, David
- Annals of Surgical Oncology, Vol. 28, Issue 2
Mitochondria and Cancer
journal, July 2016
- Vyas, Sejal; Zaganjor, Elma; Haigis, Marcia C.
- Cell, Vol. 166, Issue 3
Mitochondria and Cancer
journal, October 2015
- St. Clair, Daret
- Free Radical Biology and Medicine, Vol. 87
Loss of p53 causes mitochondrial DNA depletion and altered mitochondrial reactive oxygen species homeostasis
journal, May 2009
- Lebedeva, Maria A.; Eaton, Jana S.; Shadel, Gerald S.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1787, Issue 5
Genetic insights into OXPHOS defect and its role in cancer
journal, June 2011
- Chandra, Dhyan; Singh, Keshav K.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1807, Issue 6
Mitochondrial DNA mutations and breast tumorigenesis
journal, December 2013
- Yadav, Neelu; Chandra, Dhyan
- Biochimica et Biophysica Acta (BBA) - Reviews on Cancer, Vol. 1836, Issue 2
TZDs reduce mitochondrial ROS production and enhance mitochondrial biogenesis
journal, January 2009
- Fujisawa, Kazuo; Nishikawa, Takeshi; Kukidome, Daisuke
- Biochemical and Biophysical Research Communications, Vol. 379, Issue 1
Investigations of the potential effects of phosphorylation of the MWFE and ESSS subunits on complex I activity and assembly
journal, January 2008
- Yadava, N.; Potluri, P.; Scheffler, I. E.
- The International Journal of Biochemistry & Cell Biology, Vol. 40, Issue 3
4E-BP Extends Lifespan upon Dietary Restriction by Enhancing Mitochondrial Activity in Drosophila
journal, October 2009
- Zid, Brian M.; Rogers, Aric N.; Katewa, Subhash D.
- Cell, Vol. 139, Issue 1
Hallmarks of Cancer: The Next Generation
journal, March 2011
- Hanahan, Douglas; Weinberg, Robert A.
- Cell, Vol. 144, Issue 5
Cardiolipin and the Nlrp3 Inflammasome
journal, November 2013
- O’Neill, Luke A. J.
- Cell Metabolism, Vol. 18, Issue 5
Human OXR1 maintains mitochondrial DNA integrity and counteracts hydrogen peroxide-induced oxidative stress by regulating antioxidant pathways involving p21
journal, December 2014
- Yang, Mingyi; Luna, Luisa; Sørbø, Jan Gunnar
- Free Radical Biology and Medicine, Vol. 77
Dangerous Liaisons: Mitochondrial DNA Meets the NLRP3 Inflammasome
journal, March 2012
- Martinon, Fabio
- Immunity, Vol. 36, Issue 3
Resveratrol depletes mitochondrial DNA and inhibition of autophagy enhances resveratrol-induced caspase activation
journal, September 2013
- Prabhu, Varun; Srivastava, Pragya; Yadav, Neelu
- Mitochondrion, Vol. 13, Issue 5
Mitochondrial and postmitochondrial survival signaling in cancer
journal, May 2014
- Yadav, Neelu; Chandra, Dhyan
- Mitochondrion, Vol. 16
Mitochondria: gatekeepers of response to chemotherapy
journal, December 2013
- Sarosiek, Kristopher A.; Ni Chonghaile, Triona; Letai, Anthony
- Trends in Cell Biology, Vol. 23, Issue 12
Chinese hamster cell mutant with defective mitochondrial protein synthesis
journal, July 1977
- Ditta, G.; Soderberg, K.; Scheffler, I. E.
- Nature, Vol. 268, Issue 5615
Human mitochondrial DNA deletions associated with mutations in the gene encoding Twinkle, a phage T7 gene 4-like protein localized in mitochondria
journal, July 2001
- Spelbrink, Johannes N.; Li, Fang-Yuan; Tiranti, Valeria
- Nature Genetics, Vol. 28, Issue 3
Selective anticancer strategies via intervention of the death pathways relevant to cell transformation
journal, April 2008
- Li, Q-X; Yu, D. H.; Liu, G.
- Cell Death & Differentiation, Vol. 15, Issue 8
Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks
journal, March 2012
- Trapnell, Cole; Roberts, Adam; Goff, Loyal
- Nature Protocols, Vol. 7, Issue 3
Mitochondria and cancer
journal, September 2012
- Wallace, Douglas C.
- Nature Reviews Cancer, Vol. 12, Issue 10
Mitochondrial DNA determines the cellular response to cancer therapeutic agents
journal, November 1999
- Singh, Keshav K.; Russell, James; Sigala, Barbara
- Oncogene, Vol. 18, Issue 48
Induction of regulatory T cells by macrophages is dependent on production of reactive oxygen species
journal, September 2010
- Kraaij, Marina D.; Savage, Nigel D. L.; van der Kooij, Sandra W.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 41
Discrete mechanisms of mTOR and cell cycle regulation by AMPK agonists independent of AMPK
journal, January 2014
- Liu, X.; Chhipa, R. R.; Pooya, S.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 4
The NDUFA1 gene product (MWFE protein) is essential for activity of complex I in mammalian mitochondria
journal, April 1999
- Au, H. C.; Seo, B. B.; Matsuno-Yagi, A.
- Proceedings of the National Academy of Sciences, Vol. 96, Issue 8
Induction of a Caspase-3-like Activity by Calcium in Normal Cytosolic Extracts Triggers Nuclear Apoptosis in a Cell-free System
journal, July 1998
- Juin, Philippe; Pelletier, Maude; Oliver, Lisa
- Journal of Biological Chemistry, Vol. 273, Issue 28
Mitochondrial Dysfunction Impairs Tumor Suppressor p53 Expression/Function
journal, April 2011
- Compton, Shannon; Kim, Chul; Griner, Nicholas B.
- Journal of Biological Chemistry, Vol. 286, Issue 23
Early Mitochondrial Activation and Cytochrome c Up-regulation during Apoptosis
journal, October 2002
- Chandra, Dhyan; Liu, Jun-Wei; Tang, Dean G.
- Journal of Biological Chemistry, Vol. 277, Issue 52
Lipopolysaccharide Stimulates Mitochondrial Biogenesis via Activation of Nuclear Respiratory Factor-1
journal, August 2003
- Suliman, Hagir B.; Carraway, Martha S.; Welty-Wolf, Karen E.
- Journal of Biological Chemistry, Vol. 278, Issue 42
Mitochondrial reactive oxygen species promote production of proinflammatory cytokines and are elevated in TNFR1-associated periodic syndrome (TRAPS)
journal, January 2011
- Bulua, Ariel C.; Simon, Anna; Maddipati, Ravikanth
- The Journal of Experimental Medicine, Vol. 208, Issue 3
Regulation of the Intrinsic Apoptosis Pathway by Reactive Oxygen Species
journal, August 2013
- Wu, Chu-Chiao; Bratton, Shawn B.
- Antioxidants & Redox Signaling, Vol. 19, Issue 6
Composition and Dynamics of Human Mitochondrial Nucleoids
journal, April 2003
- Garrido, Nuria; Griparic, Lorena; Jokitalo, Eija
- Molecular Biology of the Cell, Vol. 14, Issue 4
Real time quantitative PCR.
journal, October 1996
- Heid, C. A.; Stevens, J.; Livak, K. J.
- Genome Research, Vol. 6, Issue 10, p. 986-994
DNA Polymerase γ, The Mitochondrial Replicase
journal, June 2004
- Kaguni, Laurie S.
- Annual Review of Biochemistry, Vol. 73, Issue 1
BAX supports the mitochondrial network, promoting bioenergetics in nonapoptotic cells
journal, June 2011
- Boohaker, Rebecca J.; Zhang, Ge; Carlson, Adina Loosley
- American Journal of Physiology-Cell Physiology, Vol. 300, Issue 6
Bcl-2 Inhibitors: Targeting Mitochondrial Apoptotic Pathways in Cancer Therapy
journal, February 2009
- Kang, M. H.; Reynolds, C. P.
- Clinical Cancer Research, Vol. 15, Issue 4
Defects in mitochondrial metabolism and cancer
journal, July 2014
- Gaude, Edoardo; Frezza, Christian
- Cancer & Metabolism, Vol. 2, Issue 1
p53 regulates mtDNA copy number and mitocheckpoint pathway
journal, January 2009
- Singh, KeshavK; Kulawiec, Mariola; Ayyasamy, Vanniarajan
- Journal of Carcinogenesis, Vol. 8, Issue 1
ROS-mediated mechanisms of autophagy stimulation and their relevance in cancer therapy
journal, October 2010
- Dewaele, Michael; Maes, Hannelore; Agostinis, Patrizia
- Autophagy, Vol. 6, Issue 7
Works referencing / citing this record:
Metabolic underpinnings of leukemia pathology and treatment
journal, October 2018
- Nemkov, Travis; D'Alessandro, Angelo; Reisz, Julie A.
- CANCER REPORTS, Vol. 2, Issue 2
Reactive oxygen species (ROS) are a key determinant of cancer's metabolic phenotype: ROS are a key determinant of cancer's metabolic phenotype
journal, October 2017
- Rodic, Stefan; Vincent, Mark David
- International Journal of Cancer, Vol. 142, Issue 3
Identification of novel prognostic alternative splicing signature in papillary renal cell carcinoma
journal, August 2019
- Duan, Yi; Zhang, Dong
- Journal of Cellular Biochemistry, Vol. 121, Issue 1
The Lipid Side of Bone Marrow Adipocytes: How Tumor Cells Adapt and Survive in Bone
journal, June 2018
- Diedrich, Jonathan D.; Herroon, Mackenzie K.; Rajagurubandara, Erandi
- Current Osteoporosis Reports, Vol. 16, Issue 4
Cytotoxic effect of Semialarium mexicanum (Miers) Mennega root bark extracts and fractions against breast cancer cells
journal, July 2018
- Maldonado-Cubas, Juan; San Martin-Martínez, Eduardo; Quiroz-Reyes, Cinthya Nathaly
- Physiology and Molecular Biology of Plants, Vol. 24, Issue 6
Bile acid-induced “Minority MOMP” promotes esophageal carcinogenesis while maintaining apoptotic resistance via Mcl-1
journal, September 2019
- Xu, Yuan; Surman, Deborah R.; Diggs, Laurence
- Oncogene, Vol. 39, Issue 4
Oxidative Stress and Carcinogenesis: Potential of Phytochemicals in Breast Cancer Therapy
journal, January 2017
- Forcados, Gilead Ebiegberi; James, Dorcas Bolanle; Sallau, Abdullahi Balarabe
- Nutrition and Cancer, Vol. 69, Issue 3
Carboxyamidotriazole Synergizes with Sorafenib to Combat Non–Small Cell Lung Cancer through Inhibition of NANOG and Aggravation of Apoptosis
journal, May 2017
- Chen, Chen; Ju, Rui; Shi, Jing
- Journal of Pharmacology and Experimental Therapeutics, Vol. 362, Issue 2
Resistance to neoadjuvant chemotherapy in triple-negative breast cancer mediated by a reversible drug-tolerant state
journal, April 2019
- Echeverria, Gloria V.; Ge, Zhongqi; Seth, Sahil
- Science Translational Medicine, Vol. 11, Issue 488
Targeting Oxidatively Induced DNA Damage Response in Cancer: Opportunities for Novel Cancer Therapies
journal, January 2018
- Davalli, Pierpaola; Marverti, Gaetano; Lauriola, Angela
- Oxidative Medicine and Cellular Longevity, Vol. 2018
BA6 Induces Apoptosis via Stimulation of Reactive Oxygen Species and Inhibition of Oxidative Phosphorylation in Human Lung Cancer Cells
journal, May 2019
- Cheng, Meng-Hsuan; Huang, Hung-Ling; Lin, Yen-You
- Oxidative Medicine and Cellular Longevity, Vol. 2019
Enhanced Proapoptotic Effects of Water Dispersed Complexes of 4-Thiazolidinone-Based Chemotherapeutics with a PEG-Containing Polymeric Nanocarrier
journal, April 2019
- Kobylinska, L.; Ivasechko, I.; Skorokhyd, N.
- Nanoscale Research Letters, Vol. 14, Issue 1
Inflammation and Metabolism in Cancer Cell—Mitochondria Key Player
journal, May 2019
- Neagu, Monica; Constantin, Carolina; Popescu, Iulia Dana
- Frontiers in Oncology, Vol. 9
BAP1 Status Determines the Sensitivity of Malignant Mesothelioma Cells to Gemcitabine Treatment
journal, January 2019
- Guazzelli, Alice; Meysami, Parisa; Bakker, Emyr
- International Journal of Molecular Sciences, Vol. 20, Issue 2
Sorafenib-Induced Apoptosis in Hepatocellular Carcinoma Is Reversed by SIRT1
journal, August 2019
- Garten, Antje; Grohmann, Theresa; Kluckova, Katarina
- International Journal of Molecular Sciences, Vol. 20, Issue 16
The Lipid Side of Bone Marrow Adipocytes: How Tumor Cells Adapt and Survive in Bone
journal, June 2018
- Diedrich, Jonathan D.; Herroon, Mackenzie K.; Rajagurubandara, Erandi
- Current Osteoporosis Reports, Vol. 16, Issue 4
Investigation of Mitochondrial Metabolic Response to Doxorubicin in Prostate Cancer Cells: An NADH, FAD and Tryptophan FLIM Assay
journal, September 2017
- Alam, Shagufta Rehman; Wallrabe, Horst; Svindrych, Zdenek
- Scientific Reports, Vol. 7, Issue 1
Cytochrome c1 in ductal carcinomain situof breast associated with proliferation and comedo necrosis
journal, May 2017
- Chishiki, Mayuko; Takagi, Kiyoshi; Sato, Ai
- Cancer Science, Vol. 108, Issue 7
BA6 Induces Apoptosis via Stimulation of Reactive Oxygen Species and Inhibition of Oxidative Phosphorylation in Human Lung Cancer Cells
journal, May 2019
- Cheng, Meng-Hsuan; Huang, Hung-Ling; Lin, Yen-You
- Oxidative Medicine and Cellular Longevity, Vol. 2019
Antioxidant Effects and Mechanisms of Medicinal Plants and Their Bioactive Compounds for the Prevention and Treatment of Type 2 Diabetes: An Updated Review
journal, February 2020
- Unuofin, Jeremiah Oshiomame; Lebelo, Sogolo Lucky
- Oxidative Medicine and Cellular Longevity, Vol. 2020
Enhanced Proapoptotic Effects of Water Dispersed Complexes of 4-Thiazolidinone-Based Chemotherapeutics with a PEG-Containing Polymeric Nanocarrier
journal, April 2019
- Kobylinska, L.; Ivasechko, I.; Skorokhyd, N.
- Nanoscale Research Letters, Vol. 14, Issue 1
Macrophage Migration Inhibitory Factor Secretion Is Induced by Ionizing Radiation and Oxidative Stress in Cancer Cells
journal, January 2016
- Gupta, Yashi; Pasupuleti, Vinay; Du, Weinan
- PLOS ONE, Vol. 11, Issue 1
Impact of Mediterranean diet on metabolic syndrome, cancer and longevity
journal, November 2016
- Di Daniele, Nicola; Noce, Annalisa; Vidiri, Maria Francesca
- Oncotarget, Vol. 8, Issue 5
Correction: p53 and metabolism: from mechanism to therapeutics
journal, September 2018
- Simabuco, Fernando M.; Morale, Mirian G.; Pavan, Isadora C. B.
- Oncotarget, Vol. 9, Issue 74
Inflammation and Metabolism in Cancer Cell—Mitochondria Key Player
journal, May 2019
- Neagu, Monica; Constantin, Carolina; Popescu, Iulia Dana
- Frontiers in Oncology, Vol. 9
BAP1 Status Determines the Sensitivity of Malignant Mesothelioma Cells to Gemcitabine Treatment
journal, January 2019
- Guazzelli, Alice; Meysami, Parisa; Bakker, Emyr
- International Journal of Molecular Sciences, Vol. 20, Issue 2
Ginsenoside Rh2 and Rg3 inhibit cell proliferation and induce apoptosis by increasing mitochondrial reactive oxygen species in human leukemia Jurkat cells
journal, April 2017
- Xia, Ting; Wang, Ying-Nan; Zhou, Chuan-Xin
- Molecular Medicine Reports, Vol. 15, Issue 6