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Mechanisms of cisplatin ototoxicity: theoretical review

Published online by Cambridge University Press:  07 May 2013

M S Gonçalves ,
A F Silveira ,
A R Teixeira  and
M A Hyppolito
M S Gonçalves*
Affiliation:
Department of Speech-Language Pathology and Audiology, Federal University of Santa Maria, Porto Alegre, Brazil
A F Silveira
Affiliation:
Department of Morphology/Health Sciences Center, Federal University of Santa Maria, Porto Alegre, Brazil
A R Teixeira
Affiliation:
Department of Developmental Psychology and Personality, Federal University of Rio Grande do Sul, Porto Alegre, Brazil
M A Hyppolito
Affiliation:
Department of Ophthalmology, Otorhinolaryngology and Head and Neck Surgery, Ribeirão Preto Medical School, University of São Paulo, Brazil
*
Address for correspondence: Dr Maiara S Gonçalves, Avenida Evaldo Behr, 02 Parque Residencial Novo Horizonte, Bairro Camobi, Santa Maria, RS 97110-801, Brazil Fax: +55 55 3301 1166 E-mail: [email protected]
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Abstract

Introduction:

Cisplatin is an effective chemotherapeutic agent commonly used in the treatment of malignant tumours, but ototoxicity is a significant side effect.

Objectives:

To discuss the mechanisms of cisplatin ototoxicity and subsequent cell death, and to present the results of experimental studies.

Material and methods:

We conducted a systematic search for data published in national and international journals and books, using the Medline, SciELO, Bireme, LILACS and PubMed databases.

Results:

The nicotinamide adenine dinucleotide phosphate oxidase 3 isoform (also termed NOX3) seems to be the main source of reactive oxygen species in the cochlea. These reactive oxygen species react with other molecules and trigger processes such as lipid peroxidation of the plasma membrane and increases in expression of the transient vanilloid receptor potential 1 ion channel.

Conclusion:

Cisplatin ototoxicity proceeds via the formation of reactive oxygen species in cochlear tissue, with apoptotic cell death as a consequence.

Keywords

ToxicityCisplatinCochleaHearing LossFree Radicals
Type
Review Articles
Information
The Journal of Laryngology & Otology , Volume 127 , Issue 6 , June 2013 , pp. 536 - 541
Copyright
Copyright © JLO (1984) Limited 2013 

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References

1Wang, D, Lippard, SJ. Cellular processing of platinum anticancer drugs. Nat Rev Drug Discov 2005;4:307–20CrossRefGoogle ScholarPubMed
2Jordan, JA, Schwade, ND, Truelson, JM. Fosfomycin does not inhibit the tumoricidal efficacy of cisplatinum. Laryngoscope 1999;109:1259–62CrossRefGoogle Scholar
3Hyppolito, MA, Oliveira, JA. Ototoxicity, otoprotection and self defense of the cochlear outer hair cells [in Brazilian Portuguese]. Medicina (Ribeirão Preto) 2005;38:279–89CrossRefGoogle Scholar
4Saleh, S, El-Demerdash, E. Protective effects of L-arginine against cisplatin-induced renal oxidative stress and toxicity: role of nitric oxide. Basic Clin Pharmacol Toxicol 2005;97:91–7CrossRefGoogle ScholarPubMed
5Bates, DE, Beaumont, SJ, Baylis, BW. Ototoxicity induced by gentamicin and furosemide. Ann Pharmacother 2002;36:446–51CrossRefGoogle ScholarPubMed
6Ilha, L, Kasse, C, Mesquita Neto, O, Almeida, CR, Cruz, OLM. Cisplatin-induced ototoxicity in guinea pigs: dose-related effects – a functional evaluation [in Brazilian Portuguese]. ACTA ORL/Técnicas em Otorrinolaringologia 2007;25:112–18Google Scholar
7Rybak, LP, Mukherjea, D, Jajoo, S, Ramkumar, V. Cisplatin ototoxicity and protection: clinical and experimental studies. Tohoku J Exp Med 2009;219:177–86CrossRefGoogle ScholarPubMed
8Rybak, LP, Kelly, T. Ototoxicity: bioprotective mechanisms. Curr Opin Otolaryngol Head Neck Surg 2003;11:328–33CrossRefGoogle ScholarPubMed
9Schweitzer, VG. Cisplatin-induced ototoxicity: the effect of pigmentation and inhibitory agents. Laryngoscope 1993;103:1–52Google ScholarPubMed
10Hinojosa, R, Riggs, LC, Strauss, M, Matz, GJ. Temporal bone histopathology of cisplatin ototoxicity. Am J Otol 1995;16:731–41Google ScholarPubMed
11Lee, JE, Nakagawa, T, Kita, T, Kim, TS, Iguchi, F, Endo, T et al. Mechanisms of apoptosis induced by cisplatin in marginal cells in mouse stria vascularis. ORL J Otorhinolaryngol Relat Spec 2004;66:111–18CrossRefGoogle ScholarPubMed
12Comis, SD, Rhys-Evans, PH, Osborne, MP, Pickles, JO, Jeffries, DJR, Pearse, HAC. Early morphological and chemical changes induced by cisplatin in the guinea pig organ of Corti. J Laryngol Otol 1986;100:1375–83CrossRefGoogle ScholarPubMed
13Estrem, SA, Babin, RW, Ryu, JH, Moore, KC. Cis-Diamminedichloroplatinum (II) ototoxicity in the guinea pig. Otolaryngol Head Neck Surg 1981;89:638–45CrossRefGoogle ScholarPubMed
14Feghali, JG, Lefebvre, PP, Staecker, H, Kopke, R, Frenz, DA, Malgrange, B et al. Mammalian auditory hair cell regeneration/repair and protection: a review and future directions. Ear Nose Throat J 1998;77:276–85CrossRefGoogle ScholarPubMed
15Simon, T, Hero, B, Dupuis, W, Selle, B, Berthold, F. The incidence of hearing impairment after successful treatment of neuroblastoma. Klin Pediatr 2002;214:149–52CrossRefGoogle ScholarPubMed
16Casares, C, Ramírez-Camacho, R, Trinidad, A, Roldán, A, Jorge, E, García-Berrocal, JR. Reactive oxygen species in apoptosis induced by cisplatin: review of physiopathological mechanisms in animal models. Eur Arch Otorhinolaryngol 2012;269:2455–9CrossRefGoogle ScholarPubMed
17Stavroulaki, P, Apostolopoulos, N, Segas, J, Tsakanikos, M, Adamopoulos, G. Evoked otoacoustic emissions – an approach for monitoring cisplatin induced ototoxicity in children. Int J Pediatr Otorhinolaryngol 2001;59:47–57CrossRefGoogle ScholarPubMed
18Garcia, AP, Iório, MCM, Petrilli, AS. Audiological monitoring of cisplatin exposed patients [in Brazilian Portuguese]. Rev Bras Otorrinolaringol 2003;69:215–21CrossRefGoogle Scholar
19Li, Y, Womer, RB, Silber, JH. Predicting cisplatin ototoxicity in children: influence of age and the cumulative dose. Eur J Cancer 2004;40:2445–51CrossRefGoogle ScholarPubMed
20Schneider, CD, Oliveira, AR. Oxygen free radicals and exercise: mechanisms of synthesis and adaptation to physical training [in Brazilian Portuguese]. Rev Bras Med Esporte 2004;10:308–13CrossRefGoogle Scholar
21Ferreira, ALA, Matsubara, LS. Free radicals: concepts, diseases, defense system and oxidative stress [in Brazilian Portuguese]. Rev Assoc Med Bras 1997;43:61–8Google ScholarPubMed
22Barreiros, ALBS, David, JM, David, JP. Oxidative stress: relations between the formation of reactive species and the organism's defense [in Brazilian Portuguese]. Quim Nova 2006;29:113–23CrossRefGoogle Scholar
23Freeman, BA, Crapo, JD. Biology of disease: free radical and tissue injury. Lab Invest 1982;47:412–26Google ScholarPubMed
24Kumar, V, Abbas, AK, Fausto, N. Cellular injury, cell adaptation and cell death. In: Robbins and Cotran: Pathologic Basis of Disease, 7th edn.Philadelphia: Elsevier, 2005;11–48Google Scholar
25Ross, D, Moldeus, P. Antioxidant defense systems and oxidative stress. In: Vigo-Pelfrey, C. Membrane Lipid Oxidation. Boca Raton: CRC Press, 1991;151–70Google Scholar
26Gutteridge, JMC, Halliwell, B. Antioxidants: molecules, medicines and myths. Biochem Biophys Res Commun 2010;393:561–4CrossRefGoogle ScholarPubMed
27Rybak, LP, Husain, K, Morris, C, Whitworth, C, Somani, S. Effect of protective agents against cisplatin ototoxicity. Am J Otol 2000;21:513–20Google ScholarPubMed
28Campbell, KCM, Kalkanis, J, Glatz, FR. Ototoxicity: mechanisms, protective agents and monitoring. Curr Opin Otol Head Neck Sur 2000;8:436–40CrossRefGoogle Scholar
29Van Rujven, MWM, De Groot, JCMJ, Hendriksen, F, Smoorenburg, GF. Immunohistochemical detection of platinated DNA in the cochlea of cisplatin-treated guinea pigs. Hear Res 2005;203:112–21CrossRefGoogle Scholar
30Mukherjea, D, Jajoo, S, Whitworth, CA, Bunch, JR, Turner, JG, Rybak, LP et al. Short interfering RNA against transient receptor potential vanilloid-1 attenuates cisplatin-induced hearing loss in the rat. J Neurosci 2008;28:13056–65CrossRefGoogle ScholarPubMed
31Bánfi, B, Malgrange, B, Knisz, J, Steger, K, Dubois-Dauphin, M, Krause, K-H. NOX3, a superoxide-generating NADPH oxidase of the inner ear. J Biol Chem 2004;279:46065–72CrossRefGoogle ScholarPubMed
32Rybak, LP. Mechanisms of cisplatin ototoxicity and progress in otoprotection. Curr Opin Otolaryngol Head Neck Surg 2007;15:364–9CrossRefGoogle ScholarPubMed
33Ikeda, K, Sunose, H, Takasaka, T. Effects of free radicals on the intracellular calcium concentration in the isolated hair cell of the guinea pig cochlea. Acta Otolaryngol 1993;113:137–41CrossRefGoogle ScholarPubMed
34Pigeolet, E, Corbisier, P, Houbion, A, Lambert, D, Michiels, C, Raes, M et al. Glutathione peroxidase, superoxide dismutase and catalase inactivation by peroxides and oxygen derived free radicals. Mech Ageing Dev 1990;50:283–97CrossRefGoogle Scholar
35Caterina, MJ, Schumacher, MA, Tominaga, M, Rosen, TA, Levine, JD, Julius, D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 1997;389:816–24CrossRefGoogle ScholarPubMed
36Southall, MD, Li, T, Gharibova, LS, Pei, Y, Nicol, GD, Travers, JB. Activation of epidermal vanilloid receptor-1 induces release of proinflammatory mediators in human keratinocytes. J Pharmacol Exp Ther 2003;304:217–22CrossRefGoogle ScholarPubMed
37Zheng, J, Dai, C, Steyger, PS, Kim, Y, Vass, Z, Ren, T et al. Vanilloid receptors in hearing: altered cochlear sensitivity by vanilloids and expression of TRPV1 in the organ of corti. J Neurophysiol 2003;90:444–55CrossRefGoogle ScholarPubMed
38Devarajan, P, Savoca, M, Castaneda, MP, Park, MS, Esteban-Cruciani, N, Kalinec, G et al. Cisplatin-induced apoptosis in auditory cells: role of death receptor and mitochondrial pathways. Hear Res 2002;174:45–54CrossRefGoogle ScholarPubMed
39Ravi, R, Somani, SM, Rybak, LP. Mechanism of cisplatin ototoxicity: antioxidant system. Pharmacol Toxicol 1995;76:386–94CrossRefGoogle ScholarPubMed
40Strayer, DS, Rubin, E. Cell injury. In: Rubin, E, Gorstein, F, Rubin, R, Schwarting, R, Strayer, D. Rubin's Pathology: Clinicopathologic Foundations of Medicine, 4th edn [in Brazilian Portuguese]. São Paulo: Guanabara-Koogan, 2006;2–39Google Scholar
41Hengartner, MO. The biochemistry of apoptosis. Nature 2000;407:770–6CrossRefGoogle ScholarPubMed
42Huang, T, Cheng, AG, Stupak, H, Liu, W, Kim, A, Staecker, H et al. Oxidative stress-induced apoptosis of cochlear sensory cells: otoprotective strategies. Int J Dev Neurosci 2000;18:259–70CrossRefGoogle ScholarPubMed
43Adams, JM, Cory, S. The Bcl-2 protein family: arbiters of cell death. Science 1998;281:1322–6CrossRefGoogle Scholar
44Strasser, A, O'Connor, L, Dixit, VM. Apoptosis signaling. Annu Rev Biochem 2000;69:217–45CrossRefGoogle ScholarPubMed
45Boatright, KM, Salvesen, GS. Mechanisms of caspase activation. Curr Opin Cell Biol 2003;15:725–31CrossRefGoogle ScholarPubMed
46Sharifia, AM, Eslami, H, Larijani, B, Davoodi, J. Involvement of caspase-8, 9, and 3 in high glucose-induced apoptosis in PC12 cells. Neurosci Lett 2009;459:47–51CrossRefGoogle Scholar
47Grivicich, I, Regner, A, Rocha, AB. Apoptosis: programmed cell death [in Brazilian Portuguese]. Rev Bras Cancerol 2007;53:335–43CrossRefGoogle Scholar
48Harris, MH, Thompson, CB. The role of the Bcl-2 family in the regulation of outer mitochondrial membrane permeability. Cell Death Differ 2000;7:1182–91CrossRefGoogle ScholarPubMed
49Borner, C. The Bcl-2 protein family: sensors and checkpoints for life-or-death decisions. Mol Immunol 2003;39:615–47CrossRefGoogle ScholarPubMed
50Golstein, JC, Waterhouse, NJ, Juin, P, Evan, GI, Green, DR. The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant. Nature Cell Biol 2000;2:156–62CrossRefGoogle Scholar
51Thornberry, NA, Lazebnik, Y. Caspases: enemies within. Science 1998;281:1312–16CrossRefGoogle Scholar
52Amarante-Mendes, GP, Green, DR. The regulation of apoptotic cell death. Braz J Med Biol Res 1999;32:1053–61CrossRefGoogle ScholarPubMed
53Paronlin, MB, Reason, IJ. Apoptosis as a mechanism of tissue injury in hepatobiliary diseases [in Brazilian Portuguese]. Arq Gastroenterol São Paulo 2001;38:38–44Google Scholar
54Alam, SA, Ikeda, K, Oshima, T, Suzuki, M, Kawase, T, Kikuchi, T et al. Cisplatin-induced apoptotic cell death in Mongolian gerbil cochlea. Hear Res 2000;141:28–38CrossRefGoogle ScholarPubMed
55Liu, W, Staecker, H, Stupak, H, Malgrange, B, Lefebvre, P, Van De Water, TR. Caspase inhibitors prevent cisplatin-induced apoptosis of auditory sensory cells. Neuroreport 1998;9:2609–14CrossRefGoogle ScholarPubMed
56Cheng, PW, Liu, SH, Hsu, CJ, Lin-Shiau, SY. Correlation of increased activities of Na + , K + -ATP-ase and Ca2 + -ATPase with the reversal of cisplatin ototoxicity induced by D-methionine in guinea pigs. Hear Res 2005;205:102–9CrossRefGoogle Scholar
57Cardinaal, RM, de Groot, JC, Huizing, EH, Veldman, JE, Smoorenburg, GF. Histological effects of co-administration of an ACTH(4-9) analog ORG 2766 on cisplatin ototoxicity in the albino guinea pig. Hear Res 2000;144:157–67CrossRefGoogle ScholarPubMed
58Kasse, CA, Hyppolito, MA, Cruz, OLM, Oliveira, JAA. Ototoxicity and otoprotection [in Brazilian Portuguese]. Rev Bras Med Otorrinolaringol 2008;4:105–15Google Scholar
59Rybak, L, Whitworth, C, Somani, S. Application of antioxidants and other agents to prevent cisplatin ototoxicity. Laryngoscope 1999;109:1740–4CrossRefGoogle ScholarPubMed
60Freitas, MR, Figueiredo, AA, Brito, GAC, Leitão, RFC, Carvalho, JV Jr, Gomes, RM Jr et al. The role of apoptosis in cisplatin-induced ototoxicity in rats [in Brazilian Portuguese]. Braz J Otorhinolaryngol 2009;75:745–52Google ScholarPubMed
61Sha, SH, Taylor, R, Forge, A, Schacht, J. Differential vulnerability of basal and apical hair cells is based on intrinsic susceptibility to free radicals. Hear Res 2001;155:1–8CrossRefGoogle ScholarPubMed
62Usami, S, Hjelle, OP, Ottersen, OP. Differential cellular distribution of glutathione – an endogenous antioxidant – in the guinea pig inner ear. Brain Res 1996;743:337–40CrossRefGoogle ScholarPubMed
63Muldoon, LL, Pagel, MA, Kroll, RA, Brummett, RE, Doolittle, ND, Zuhowski, EG et al. Delayed administration of sodium thiosulfate in animal models reduces platinum ototoxicity without reduction of antitumor activity. Clin Cancer Res 2000;6:309–15Google ScholarPubMed
64Hyppolito, MA, Oliveira, JAA, Lessa, RM, Rossato, M. Amifostine otoprotection to cisplatin ototoxicity: a guinea pig study using otoacoustic emission distortion products (DPOEA) and scanning electron microscopy [in Brazilian Portuguese]. Rev Bras Otorrinolaringol 2005;71:168–273Google ScholarPubMed
65Hyppolito, MA, Oliveira, JAA, Rossato, M, Holanda, F. Cisplatin ototoxicity and otoprotector to ciliated cells by ginkgo biloba extract: anatomic and electrophysiologic study [in Brazilian Portuguese]. Rev Bras Otorrinolaringol 2003;69:504–11CrossRefGoogle Scholar
66Kalkanis, JG, Whitworth, C, Rybak, LP. Vitamin E reduces cisplatin ototoxicity. Laryngoscope 2004;114:538–42CrossRefGoogle ScholarPubMed
67Feghali, JG, Liu, W, Van De Water, TR. L-N-acetyl-cysteine protection against cisplatin-induced auditory neuronal and hair cell toxicity. Laryngoscope 2001;111:1147–55CrossRefGoogle ScholarPubMed
68Fetoni, AR, Ralli, M, Sergi, B, Parrilla, C, Troiani, D, Paludetti, G. Protective effects of N-acetylcysteine on noise-induced hearing loss in guinea pigs. Acta Otorhinolaryngol Ital 2009;29:70–5Google ScholarPubMed
69Riga, MG, Chelis, L, Kakolyris, S, Papadopoulos, S, Stathakidou, S, Chamalidou, E et al. Transtympanic injections of N-acetylcysteine for the prevention of cisplatin-induced ototoxicity: a feasible method with promising efficacy. Am J Clin Oncol 2013;36:1–6CrossRefGoogle ScholarPubMed