Highlights
- •Reactive oxygen species release increases in cisplatin-treated zebrafish endorgans.
- •Reactive oxygen species production in cisplatin only samples is dosage dependent.
- •Curcuminoid treatment does not increase endorgan reactive oxygen species.
- •Curcuminoid treatment counteracts cisplatin reactive oxygen species production.
Abstract
Cisplatin is a widely used chemotherapy drug that can damage auditory and vestibular
tissue and cause hearing and balance loss through the intracellular release of reactive
oxygen species (ROS). Curcumin has anticancer efficacy and can also counteract cisplatin’s
damaging effect against sensory tissue by scavenging intracellular ROS, but curcumin’s
applicability is limited due to its low bioavailability. EF-24 is a synthetic curcumin
analog that is more bioavailable than curcumin and can target cancer, but its effects
against cisplatin-mediated ROS in auditory and vestibular tissue is currently unknown.
In this study, we employed a novel zebrafish inner ear tissue culture system to determine
if EF-24 counteracted cisplatin-mediated ROS release in two sensory endorgans, the
saccule and the utricle. The zebrafish saccule is associated with auditory function
and the utricle with vestibular function. Trimmed endorgans were placed in tissue
culture media with a fluorescent reactive oxygen species indicator dye, and intracellular
ROS release was measured using a spectrophotometer. We found that cisplatin treatment
significantly increased ROS compared to controls, but that EF-24 treatment did not
alter or even decreased ROS. Importantly, when equimolar cisplatin and EF-24 treatments
are combined, ROS did not increase compared to controls. This suggests that EF-24
may be able to prevent intracellular ROS caused by cisplatin treatment in inner ear
tissue.
Keywords
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References
- Human colon cancer cells surviving high doses of cisplatin or oxaliplatin in vitro are not defective in DNA mismatch repair proteins.Cancer Chemother Pharmacol. 2002; 49: 445-452
- Biochemical mechanisms of cisplatin cytotoxicity.Anticancer Agents Med Chem. 2007; 7: 3-18
- Chromatin status of apoptosis genes correlates with sensitivity to chemo-, immune- and radiation therapy in colorectal cancer cell lines.Apoptosis. 2014; 19: 1769-1778
- Attenuation of cisplatin ototoxicity by otoprotective effects of nanoencapsulated curcumin and dexamethasone in a guinea pig model.Otol Neurotol. 2014; 35: 1131-1139
- An integrated view of cisplatin-induced nephrotoxicity and ototoxicity.Toxicol Lett. 2015; 237: 219-227
- Cisplatin-induced ototoxicity: effect of intratympanic dexamethasone injections.Otol Neurotol. 2008; 29: 1005-1011
- A combination of cilostazol and Ginkgo biloba extract protects against cisplatin-induced Cochleo-vestibular dysfunction by inhibiting the mitochondrial apoptotic and ERK pathways.Cell Death Dis. 2013; 4e509https://doi.org/10.1038/cddis.2013.33
- Behavioral changes of zebrafish according to cisplatin-induced toxicity of the balance system.Hum Exp Toxicol. 2014; 33: 1167-1175
- Allicin protects against cisplatin-induced vestibular dysfunction by inhibiting the apoptotic pathway.Eur J Pharmacol. 2017; 805: 108-117
- The multifaceted role of curcumin in cancer prevention and treatment.Molecules. 2015; 20: 2728-2769
- Hybrid curcumin compounds: a new strategy for cancer treatment.Molecules. 2014; 19: 20839-20863
- Plant derived substances with anti-cancer activity: from folklore to practice.Front Plant Sci. 2015; 6: 799https://doi.org/10.3389/fpls.2015.00799
- Prevention and restoration of hearing loss associated with the use of cisplatin.Biomed Res Int. 2014; : 925485https://doi.org/10.1155/2014/925485
- Multiple anticancer activities of EF24, a novel curcumin analog, on human ovarian carcinoma cells.Reprod Sci. 2010; 17: 931-940
- Reactive oxygen species in apoptosis induced by cisplatin: review of physiopathological mechanisms in animal models.Eur Arch Otorhinolaryngol. 2012; 269: 2455-2459
- Distinct subpopulations of head and neck cancer cells with different levels of intracellular reactive oxygen species exhibit diverse stemness, proliferation, and chemosensitivity.Cancer Res. 2014; 74: 6291-6305
- New perspectives of curcumin in cancer prevention.Cancer Prev Res (Phila). 2013; 6: 387-400
- Natural compounds modulating mitochondrial functions.Evid Based Complement Alternat Med. 2015; : 527209https://doi.org/10.1155/2015/527209
- Recent developments in curcumin and curcumin based polymeric materials for biomedical applications: a review.Int J Biol Macromol. 2015; 81: 877-890
- Potential anticancer properties and mechanisms of action of curcumin.Anticancer Res. 2015; 35: 645-651
- Synthesis and biological evaluation of novel curcumin analogs as anti-cancer and anti-angiogenesis agents.Bioorg Med Chem. 2004; 12: 3871-3883
- Synthesis and biological evaluation of aromatic enones related to curcumin.Bioorg Med Chem. 2005; 13: 4007-4013
- Anticancer activities of novel chalcone and bis-chalcone derivatives.Bioorg Med Chem. 2006; 14: 3491-3495
- CLEFMA-an anti-proliferative curcuminoid from structure-activity relationship studies on 3,5-bis(benzylidene)-4-piperidones.Bioorg Med Chem. 2010; 18: 6109-6120
- Pharmacologic suppression of inflammation by a diphenyldifluoroketone, EF24, in a rat model of fixed-volume hemorrhage improves survival.Pharmacol Exp Ther. 2013; 347: 346-356
- EF24 prevents rotenone-induced estrogenic status alteration in breast cancer.Cell Biol Int. 2014; 38: 511-519
- Chemical screening for hair cell loss and protection in the zebrafish lateral line.Zebrafish. 2010; 7: 3-11
- Drug screening for hearing loss: using the zebrafish lateral line to screen for drugs that prevent and cause hearing loss.Drug Discov Today. 2010; 15: 265-271
- Screening for chemicals that affect hair cell death and survival in the zebrafish lateral line.Hear Res. 2012; 288: 58-66
- Sensory hair cell death and regeneration in fishes.Front Cell Neurosci. 2015; 9: 131https://doi.org/10.3389/fncel.2015.00131
- Using the zebrafish lateral line to uncover novel mechanisms of action and prevention in drug-induced hair cell death.Front Cell Neurosci. 2015; 9: 46https://doi.org/10.3389/fncel.2015.00046
- Mitochondrial calcium uptake underlies ROS generation during aminoglycoside-induced hair cell death.J Clin Invest. 2016; 126: 3556-3566
- Functional mechanotransduction is required for cisplatin-induced hair cell death in the zebrafish lateral line.J Neurosci. 2013; 33: 4405-4414
- Aminoglycoside-induced hair cell death of inner ear organs causes functional deficits in adult zebrafish (Danio rerio).PLoS One. 2013; 8: e58755https://doi.org/10.1371/journal.pone.0058755
- Development of a respiratory burst assay using zebrafish kidneys and embryos.J Immunol Methods. 2004; 292: 119-129
- Selective anticancer copper(II)-mixed ligand complexes: targeting of ROS and proteasomes.Metallomics. 2014; 6: 892-906
- Sound detection and processing by fish: critical review and major research questions.Brain Behav Evol. 1993; 41: 14-38
- Ontogenetic development of the auditory sensory organ in zebrafish (Danio rerio): changes in hearing sensitivity and related morphology.Sci Rep. 2015; 5: 15943https://doi.org/10.1038/srep15943
- The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish.4th ed. Institute of Neuroscience, University of Oregon, Eugene1994
- Growth hormone promotes hair cell regeneration in the zebrafish (Danio rerio) inner ear following acoustic trauma.PLoS ONE. 2011; 6e28372https://doi.org/10.1371/journal.pone.0028372
- Structure, recognition, and processing of cisplatin-DNA adducts.Chem Rev. 1999; 99: 2467-2498
- Enhancement of cisplatin cytotoxicity by terbium in cisplatin-resistant MDA/CH human breast cancer cells.Cancer Chemother Pharmacol. 1999; 44: 249-252
- Systems modeling accurately predicts responses to genotoxic agents and their synergism with BCL-2 inhibitors in triple negative breast cancer cells.Cell Death Dis. 2018; 9: 42https://doi.org/10.1038/s41419-017-0039-y
- Non-DNA-binding platinum anticancer agents: cytotoxic activities of platinum–phosphato complexes towards human ovarian cancer cells.Proc Natl Acad Sci U S A. 2008; 105: 18314-18319
- Say no to DMSO: dimethylsulfoxide inactivates cisplatin, carboplatin, and other platinum complexes.Cancer Res. 2014; 74: 3913-3922
- EF24 and RAD001 potentiates the anticancer effect of platinum-based agents in human malignant pleural mesothelioma (MSTO-211H) cells and protects nonmalignant mesothelial (MET-5A) cells.Hum Exp Toxicol. 2015; 34: 117-126
- Synergistic antitumor activity of rapamycin and EF24 via increasing ROS for the treatment of gastric cancer.Redox Biol. 2016; 10: 78-89
- EF24 induces ROS-mediated apoptosis via targeting thioredoxin reductase 1 in gastric cancer cells.Oncotarget. 2016; 7: 18050-18064
- Curcumin analog EF24 induces apoptosis via ROS-dependent mitochondrial dysfunction in human colorectal cancer cells.Cancer Chemother Pharmacol. 2016; 78: 1151-1161
- Curcuminoid EF24 enhances the anti-tumour activity of Akt inhibitor MK-2206 through ROS-mediated endoplasmic reticulum stress and mitochondrial dysfunction in gastric cancer.Br J Pharmacol. 2017; 174: 1131-1146
- The curcuminoid CLEFMA selectively induces cell death in H441 lung adenocarcinoma cells via oxidative stress.Invest New Drugs. 2012; 30: 558-567
- Cytotoxicity, ROS-generation activity and radical-scavenging activity of curcumin and related compounds.Anticancer Res. 2004; 24: 563-569
- Intracellular ROS protection efficiency and free radical-scavenging activity of curcumin.PLoS One. 2011; 6: e26012https://doi.org/10.1371/journal.pone.0026012
- Pharmacogenomics of cisplatin-induced ototoxicity.Pharmacogenomics. 2011; 12: 1039-1050https://doi.org/10.2217/pgs.11.48
Article info
Publication history
Published online: September 19, 2018
Accepted:
September 10,
2018
Received:
May 21,
2018
Identification
Copyright
© 2018 Elsevier Ltd. All rights reserved.
