Deciphering the molecular mechanism during doxorubicin-mediated oxidative stress, apoptosis through Nrf2 and PGC-1α in a rat testicular milieu

Damiani, 2016, Pathways of cardiac toxicity: comparison between chemotherapeutic drugs doxorubicin and mitoxantrone, Arch Toxicol, 90, 2063, 10.1007/s00204-016-1759-y

Zhang, 2012, Identification of the molecular basis of doxorubicin-induced cardiotoxicity, Nat Med, 18, 1639, 10.1038/nm.2919

Renu, 2017, Molecular mechanism of doxorubicin-induced cardiomyopathy–An update, Eur J Pharmacol

Renu, 2018, Elevated lipolysis in adipose tissue by doxorubicin via PPARα activation associated with hepatic steatosis and insulin resistance, Eur J Pharmacol

Arunachalam, 2013, Doxorubicin treatment inhibits PPARγ and may induce lipotoxicity by mimicking a type 2 diabetes‐like condition in rodent models, FEBS Lett, 587, 105, 10.1016/j.febslet.2012.11.019

Renu, 2017, Adriamycin-induced cardiomyopathy can serve as a model for diabetic cardiomyopathy-A hypothesis, Asian Pac J Trop Biomed, 10.1016/j.apjtb.2017.09.021

Levi, 2015, Dexrazoxane exacerbates doxorubicin-induced testicular toxicity, Reproduction, 150, 357, 10.1530/REP-15-0129

Wallace, 2011, Oncofertility and preservation of reproductive capacity in children and young adults, Cancer, 117, 2301, 10.1002/cncr.26045

Meistrich, 1990, Low levels of chromosomal mutations in germ cells derived from doxorubicin-treated stem spermatogonia in the mouse, Cancer Res, 50, 370

Renu, 2018, Review on molecular and biochemical insights of arsenic-mediated male reproductive toxicity, Life Sci, 10.1016/j.lfs.2018.09.045

Pérez, 2009, Is the oxidative stress theory of aging dead?, Biochim. Biophys., 1790, 1005, 10.1016/j.bbagen.2009.06.003

Yeh, 2009, A standardized extract of Ginkgo biloba suppresses doxorubicin‐induced oxidative stress and p53‐mediated mitochondrial apoptosis in rat testes, Br J Pharmacol, 156, 48, 10.1111/j.1476-5381.2008.00042.x

Lee, 2012, Melatonin attenuates doxorubicin‐induced testicular toxicity in rats, Andrologia, 44, 796, 10.1111/j.1439-0272.2011.01269.x

Dinkova-Kostova, 2015, The emerging role of Nrf2 in mitochondrial function, Free Radic Biol Med, 88, 179, 10.1016/j.freeradbiomed.2015.04.036

Anderson, 2008, Dynamic regulation of PGC‐1α localization and turnover implicates mitochondrial adaptation in calorie restriction and the stress response, Aging Cell, 7, 101, 10.1111/j.1474-9726.2007.00357.x

Valle, 2005, PGC-1α regulates the mitochondrial antioxidant defense system in vascular endothelial cells, Cardiovasc Res, 66, 562, 10.1016/j.cardiores.2005.01.026

St-Pierre, 2006, Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators, Cell, 127, 397, 10.1016/j.cell.2006.09.024

Brand, 2000, Uncoupling to survive? The role of mitochondrial inefficiency in aging, Exp Gerontol, 35, 811, 10.1016/S0531-5565(00)00135-2

Thackaberry, 2005, Toxicogenomic profile of 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin in the murine fetal heart: modulation of cell cycle and extracellular matrix genes, Toxicol Sci, 88, 231, 10.1093/toxsci/kfi301

Matsumura, 2009, The significance of the nongenomic pathway in mediating inflammatory signaling of the dioxin-activated Ah receptor to cause toxic effects, Biochem Pharmacol, 77, 608, 10.1016/j.bcp.2008.10.013

Aitken, 2008, Antioxidant systems and oxidative stress in the testes, Oxid Med Cell Longev, 1, 15, 10.4161/oxim.1.1.6843

Rd, 2003, Expression of aryl hydrocarbon receptor and aryl hydrocarbon receptor nuclear translocator messenger ribonucleic acids and proteins in rat and human testis, Endocrinology, 144, 767, 10.1210/en.2002-220642

Piton, 2010, Involvement of pregnane X receptor in the regulation of CYP2B6 gene expression by oltipraz in human hepatocytes, Toxicol In Vitro, 24, 452, 10.1016/j.tiv.2009.09.025

Gareau, 2010, The SUMO pathway: emerging mechanisms that shape specificity, conjugatio, and recognition, Nat Rev Mol Cell Biol, 11, 861, 10.1038/nrm3011

Geiss-Friedlander, 2007, Concepts in sumoylation: a decade on, Nat Rev Mol Cell Biol, 8, 947, 10.1038/nrm2293

He, 2015, Characterization of the loss of SUMO pathway function on cancer cells and tumor proliferation, PLoS One, 10

Bebington, 2001, The possible biological and reproductive functions of ubiquitin, Hum Reprod Update, 7, 102, 10.1093/humupd/7.1.102

Sutovsky, 2003, Ubiquitin‐dependent proteolysis in mammalian spermatogenesis, fertilization, and sperm quality control: killing three birds with one stone, Microsc Res Tech, 61, 88, 10.1002/jemt.10319

Yang, 2017, Assessment of doxorubicin-induced mouse testicular damage by the novel second-harmonic generation microscopy, Am J Transl Res, 9, 5275

Ewing, 1995, Microplate superoxide dismutase assay employing a nonenzymatic superoxide generator, Anal Biochem, 232, 243, 10.1006/abio.1995.0014

Yang, 2016, Cytotoxicity of pyrrolizidine alkaloid in human hepatic parenchymal and sinusoidal endothelial cells: firm evidence for the reactive metabolites mediated pyrrolizidine alkaloid-induced hepatotoxicity, Chem Biol Interact, 243, 119, 10.1016/j.cbi.2015.09.011

Gartaganis, 2007, Evidence for oxidative stress in lens epithelial cells in pseudoexfoliation syndrome, Eye, 21, 1406, 10.1038/sj.eye.6702596

Suman, 2012, An improved non-enzymatic “DNA ladder assay” for more sensitive and early detection of apoptosis, Cytotechnology, 64, 9, 10.1007/s10616-011-9395-0

Heidari, 2016, Sulfasalazine-induced renal injury in rats and the protective role of thiol-reductants, Ren Fail, 38, 137, 10.3109/0886022X.2015.1096731

Helmy, 2018, Chloroquine upregulates TRAIL/TRAILR2 expression and potentiates doxorubicin anti-tumor activity in thioacetamide-induced hepatocellular carcinoma model, Chem Biol Interact, 279, 84, 10.1016/j.cbi.2017.11.009

Bar-Joseph, 2011, In vivo bioimaging as a novel strategy to detect doxorubicin-induced damage to gonadal blood vessels, PLoS One, 6, 10.1371/journal.pone.0023492

Kensler, 2009, Nrf2: friend or foe for chemoprevention?, Carcinogenesis, 31, 90, 10.1093/carcin/bgp231

Menegon, 2016, The dual roles of NRF2 in cancer, Trends Mol Med, 22, 578, 10.1016/j.molmed.2016.05.002

Kwak, 2010, Targeting NRF2 signaling for cancer chemoprevention, Toxicol Appl Pharmacol, 244, 66, 10.1016/j.taap.2009.08.028

Calkins, 2009, The Nrf2/ARE pathway as a potential therapeutic target in neurodegenerative disease, Antioxid Redox Signal, 11, 497, 10.1089/ars.2008.2242

Kensler, 2011, Modulation of the metabolism of airborne pollutants by glucoraphanin-rich and sulforaphane-rich broccoli sprout beverages in Qidong, China, Carcinogenesis, 33, 101, 10.1093/carcin/bgr229

Shureiqi, 2011, Curcumin chemoprevention: the long road to clinical translation, Cancer Prev Res, 4, 296, 10.1158/1940-6207.CAPR-11-0060

Linker, 2011, Fumaric acid esters exert neuroprotective effects in neuroinflammation via activation of the Nrf2 antioxidant pathway, Brain, 134, 678, 10.1093/brain/awq386

Scannevin, 2012, Fumarates promote cytoprotection of central nervous system cells against oxidative stress via the nuclear factor (erythroid-derived 2)-like 2 pathway, J Pharmacol Exp Ther, 341, 274, 10.1124/jpet.111.190132

Palsamy, 2011, Resveratrol protects diabetic kidney by attenuating hyperglycemia-mediated oxidative stress and renal inflammatory cytokines via Nrf2–Keap1 signaling, Biochim. Biophys., 1812, 719, 10.1016/j.bbadis.2011.03.008

Wang, 2008, Nrf2 enhances resistance of cancer cells to chemotherapeutic drugs, the dark side of Nrf2, Carcinogenesis, 29, 1235, 10.1093/carcin/bgn095

Yamadori, 2012, Molecular mechanisms for the regulation of Nrf2-mediated cell proliferation in non-small-cell lung cancers, Oncogene, 31, 4768, 10.1038/onc.2011.628

Sporn, 2012, NRF2 and cancer: the good, the bad and the importance of context, Nat Rev Cancer, 12, 564, 10.1038/nrc3278

Shibata, 2008, Cancer related mutations in NRF2 impair its recognition by Keap1-Cul3 E3 ligase and promote malignancy, Proc Natl Acad Sci U S A, 105, 13568, 10.1073/pnas.0806268105

Shibata, 2008, Genetic alteration of Keap1 confers constitutive Nrf2 activation and resistance to chemotherapy in gallbladder cancer, Gastroenterology, 135, e4, 10.1053/j.gastro.2008.06.082

Homma, 2009, Nrf2 enhances cell proliferation and resistance to anticancer drugs in human lung cancer, Clin Cancer Res, 15, 3423, 10.1158/1078-0432.CCR-08-2822

Jiang, 2010, High levels of Nrf2 determine chemoresistance in type II endometrial cancer, Cancer Res, 70, 5486, 10.1158/0008-5472.CAN-10-0713

Singh, 2008, RNAi-mediated silencing of nuclear factor erythroid-2–related factor 2 gene expression in non–small cell lung cancer inhibits tumor growth and increases efficacy of chemotherapy, Cancer Res, 68, 7975, 10.1158/0008-5472.CAN-08-1401

Zhou, 2016, Sulforaphane protects against rotenone-induced neurotoxicity in vivo: involvement of the mTOR, Nrf2, and autophagy pathways, Sci Rep, 6, 32206, 10.1038/srep32206

Marmolino, 2010, PGC-1alpha down-regulation affects the antioxidant response in Friedreich’s ataxia, PLoS One, 5, 10.1371/journal.pone.0010025

Qiu, 2010, Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation, Cell Metab, 12, 662, 10.1016/j.cmet.2010.11.015

Wagner, 2005, Doxorubicin increases intracellular hydrogen peroxide in PC3 prostate cancer cells, Arch Biochem Biophys, 440, 181, 10.1016/j.abb.2005.06.015

Rato, 2014, Pre-diabetes alters testicular PGC1-α/SIRT3 axis modulating mitochondrial bioenergetics and oxidative stress, Biochim Biophys Acta, 1837, 335, 10.1016/j.bbabio.2013.12.008

Krauss, 2002, A significant portion of mitochondrial proton leak in intact thymocytes depends on expression of UCP2, Proc Natl Acad Sci U S A, 99, 118, 10.1073/pnas.012410699

Amaral, 2008, Testicular aging involves mitochondrial dysfunction as well as an increase in UCP2 levels and proton leak, FEBS Lett, 582, 4191, 10.1016/j.febslet.2008.11.020

Maejima, 2008, Induction of premature senescence in cardiomyocytes by doxorubicin as a novel mechanism of myocardial damage, Aging Cell, 7, 125, 10.1111/j.1474-9726.2007.00358.x

Kuznetsov, 2011, Changes in mitochondrial redox state, membrane potential and calcium precede mitochondrial dysfunction in doxorubicin-induced cell death, Biochim Biophys Acta, 1813, 1144, 10.1016/j.bbamcr.2011.03.002

Li, 2006, An oligonucleotide microarray study on gene expression profile in mouse testis of experimental cryptorchidism, Front Biosci., 11, 2465, 10.2741/1983

Zhang, 2007, Uncoupling protein 2 protects testicular germ cells from hyperthermia-induced apoptosis, Biochem Biophys Res Commun, 360, 327, 10.1016/j.bbrc.2007.06.071

Robbins, 2011, New aspects of mitochondrial uncoupling proteins (UCPs) and their roles in tumorigenesis, Int J Mol Sci, 12, 5285, 10.3390/ijms12085285

Hansen, 2014, The aryl hydrocarbon receptor is important for proper seminiferous tubule architecture and sperm development in mice, Biol Reprod, 90, 10.1095/biolreprod.113.108845

Esakky, 2012, Cigarette smoke condensate induces aryl hydrocarbon receptor-dependent changes in gene expression in spermatocytes, Reprod Toxicol, 34, 665, 10.1016/j.reprotox.2012.10.005

Ward, 1988, Delayed effects of doxorubicin on spermatogenesis and endocrine function in rats, Reprod Toxicol, 2, 117, 10.1016/0890-6238(88)90007-X

Perdew, 1988, Association of the Ah receptor with the 90-kDa heat shock protein, J Biol Chem, 263, 13802, 10.1016/S0021-9258(18)68314-0

Heid, 2000, Role of heat shock protein 90 dissociation in mediating agonist-induced activation of the aryl hydrocarbon receptor, Mol Pharmacol, 57, 82

Chen, 1997, The Ah receptor is a sensitive target of geldanamycin-induced protein turnover, Arch Biochem Biophys, 348, 190, 10.1006/abbi.1997.0398

Gabrielson, 2007, Heat shock protein 90 and ErbB2 in the cardiac response to doxorubicin injury, Cancer Res, 67, 1436, 10.1158/0008-5472.CAN-06-3721

Whyte-Allman, 2017, Xenobiotic nuclear receptors pregnane X recepto, and constitutive androstane receptor regulate antiretroviral drug efflux transporters at the blood-testis barrier, J Pharmacol Exp Ther, 363, 324, 10.1124/jpet.117.243584

Gong, 2006, Orphan nuclear receptor pregnane X receptor sensitizes oxidative stress responses in transgenic mice and cancerous cells, Mol Endocrinol, 20, 279, 10.1210/me.2005-0205

Kakehashi, 2013, Mode of action of ethyl tertiary-butyl ether hepatotumorigenicity in the rat: evidence for a role of oxidative stress via activation of CAR, PX, and PPAR signaling pathways, Toxicol Appl Pharmacol, 273, 390, 10.1016/j.taap.2013.09.016

Yao, 2009, Testicular annexin A5 expression augmented by experimental cryptorchidism and could affect germ cell apoptosis in rats, Urology, 73, 1412, 10.1016/j.urology.2008.11.021

Kumar, 2002, Oxidative stress associated DNA damage in testis of mice: induction of abnormal sperms and effects on fertility, Mutat Res Genet Toxicol Environ Mutagen, 513, 103, 10.1016/S1383-5718(01)00300-X

Malloy, 2013, Trafficking of the transcription factor Nrf2 to promyelocytic leukemia-nuclear bodies IMPLICATIONS FOR DEGRADATION OF NRF2 IN THE NUCLEUS, J Biol Chem, 288, 14569, 10.1074/jbc.M112.437392

Vigodner, 2005, Testicular expression of small ubiquitin-related modifier-1 (SUMO-1) supports multiple roles in spermatogenesis: silencing of sex chromosomes in spermatocytes, spermatid microtubule nucleation, and nuclear reshaping, Dev Biol, 282, 480, 10.1016/j.ydbio.2005.03.034

Zebrack, 2008, The impact of cancer and quality of life for long‐term survivors, Psycho-Oncology, 17, 891, 10.1002/pon.1300