Top

European Archives of Oto-Rhino-Laryngology

Published in:

01-12-2012 | Review Article

Reactive oxygen species in apoptosis induced by cisplatin: review of physiopathological mechanisms in animal models

Authors: Celia Casares, Rafael Ramírez-Camacho, Almudena Trinidad, Amaya Roldán, Eduardo Jorge, José Ramón García-Berrocal

Published in: European Archives of Oto-Rhino-Laryngology | Issue 12/2012

Abstract

Cisplatin is a highly effective chemotherapeutic agent but displays significant ototoxic side effects. The most prominent change seen in the cochlea after cisplatin administration consists of loss of outer hair cells. Several mechanisms are believed to mediate cisplatin-induced apoptosis: binding of cisplatin to guanine bases on DNA and the formation of inter- and intra-strand chain cross-linking, generation of reactive oxygen species (ROS) with increased lipid peroxidation and Ca²⁺ influx and, finally, inflammation mediated by cisplatin. The aim of the present review is to analyze the role of ROS in the mechanisms causing cisplatin-mediated apoptosis in the inner ear and the contribution of the different pathways involved, emphasizing the main strategies to blockade events leading to apoptosis of cochlear cells.

Estrem SA, Babin RW, Ryu JH, Moore KC (1981) Cis-diamminedichloroplatinum (II) ototoxicity in the guinea pig. Otolaryngol Head Neck Surg 89:638–645PubMed

Anniko M, Sobin A (1986) Cisplatin: evaluation of its ototoxic potential. Am J Otol 7:276–293CrossRef

Watanabe K, Yagi T (2000) Expression of myeloperoxidase in the inner ear of cisplatin-treated guinea pigs. Anticancer Drugs 11:727–730PubMedCrossRef

Lee JE, Nagakawa T, Kita T, Kim TS, Iguchi F, Endo T, Shiga A, Lee SH, Ito J (2004) Mechanisms of apoptosis induced by cisplatin in marginal cells in mouse stria vascularis. ORL J Otorhinolaryngol Relat Spec 66:111–118PubMedCrossRef

Ramírez-Camacho R, García-Berrocal JR, Trinidad A, González-García JA, Verdaguer JM, Ibáñez A, Rodríguez A, Sanz R (2006) Central role of supporting cells in cochlear homeostasis and pathology. Med Hypotheses 67:550–555PubMedCrossRef

McKeage MJ (1995) Comparative adverse effect profiles of platinum drugs. Drug Saf 13:228–244PubMedCrossRef

Ashkenazi A, Dixit VM (1998) Death receptors: signalling and modulation. Science 281:1305–1308PubMedCrossRef

Harris MH, Thompson CB (2000) The role of Bcl-2 family in the regulation of outer mitochondrial membrane permeability. Cell Death Differ 7:1182–1191PubMedCrossRef

Goldstein JC, Waterhouse NJ, Juin P, Evan GI, Green DR (2000) The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant. Nature Cell Biol 2:156–162PubMedCrossRef

10.

Li H, Zhu H, Xu CJ, Yuan J (1998) Cleavage of Bid by caspase 8 mediated the mitochondrial damage in the Fas pathway of apoptosis. Cell 94:491–501PubMedCrossRef

11.

Thomas JP, Lautermann J, Liedert B, Seller F, Thomale J (2006) High accumulation of platinum-DNA adducts in strial marginal cells of the cochlea is an early event in cisplatin but not in carboplatin ototoxicity. Mol Pharmacol 70:23–29PubMed

12.

Liang F, Schulte BA, Qu C, Hu W, Shen Z (2005) Inhibition of the calcium and voltage-dependent big conductance potassium channel ameliorates cisplatin-induced apoptosis in spiral ligament fibrocytes of the cochlea. Neuroscience 135:263–271PubMedCrossRef

13.

Watanabe K, Hess A, Bloch W, Michel O (2000) Nitric oxide synthase inhibitor suppresses the ototoxic side effects of cisplatin in guinea pigs. Anticancer Drugs 11:401–406PubMedCrossRef

14.

Mukherjea D, Kaur T, Jajoo S, Sheehan KE, Ramkumar V, Rybak LP (2010) Transtympanic administration of short interfering (si)RNA for the NOX3 isoform of NADPH oxidase protects against cisplatin-induced hearing loss in the rat. Antiox Redox Signal 13(5):589–598CrossRef

15.

Rybak LP, Husain K, Whitworth C, Somani SM (1999) Dose dependent protection by lipoic acid against cisplatin ototoxicity in rats: antioxidant defense system. Toxicol Sci 47:195–202PubMedCrossRef

16.

Rybak LP (2007) Mechanisms of cisplatin ototoxicity and progress in otoprotection. Curr Opin Otolaryngol Head Neck Surg 15:364–369PubMedCrossRef

17.

González-García JA, Nevado J, García-Berrocal JR, Sánchez-Rodríguez C, Sanz R, Ramírez-Camacho R (2010) Endogenous protection against oxidative stress caused by cisplatin: role of superoxide dismutase. Acta Otolaryngol 130:453–457PubMedCrossRef

18.

Mukherjea D, Jajoo S, Whitworth C, Bunch JR, Turner JG, Rybak LP, Ramkumar B (2008) Short interfering (si)RNA against transient receptor potential Vanilloid-1 (TRPV1) attenuates cisplatin-induced hearing loss in the rat. J Neurosci 28(49):13056–13065PubMedCrossRef

19.

Rybak LP, Whitworth CA, Mukherjea D, Ramkumar V (2007) Mechanisms of cisplatin-induced ototoxicity and prevention. Hear Res 226(1–2):157–167PubMedCrossRef

20.

Xu Y, Huang S, Liu ZG, Han J (2006) Poly (ADP-ribose) polymerase-1 signalling to mitochondria in necrotic cell death requires RIP1/TRAF2-mediated JNK1 activation. J Biol Chem 281(13):8788–8795PubMedCrossRef

21.

Francis SP, Kramarenko II, Brandon CS, Lee FS, Baker TG, Cunningham LL (2011) Celastrol inhibits aminoglycoside-induced ototoxicity via heat shock protein 32. Cell Death Dis 2:e195PubMedCrossRef

22.

Kim HJ, So HS, Lee JH, Park C, Park SY, Kim YH, Youn MJ, Kim SJ, Chung SY, Lee KM, Park R (2006) Heme oxygenase-1 attenuates the cisplatin-induced apoptosis of auditory cells via down-regulation of reactive oxygen species generation. Free Radic Biol Med 40:1810–1819PubMedCrossRef

23.

Choi BM, Chen XY, Gao SS, Zhu R, Kim BR (2011) Anti-apoptotic effect of phloretin on cisplatin-induced apoptosis in HEI-OC1 auditory cells. Pharmacol Rep 63(3):708–716PubMed

24.

Cunningham LL, Brandon CS (2006) Heat shock inhibits both aminoglycoside- and cisplatin induced sensory hair cell death. J Assoc Res Otolaryngol 7:299–307PubMedCrossRef

25.

García-Berrocal JR, Nevado J, González-García JA, Sánchez-Rodríguez C, Sanz R, Trinidad A, España P, Citores MJ, Ramírez-Camacho R (2010) Heat shock protein 70 and cellular disturbances in cochlear cisplatin ototoxicity model. J Laryngol Otol 124:599–609PubMedCrossRef

26.

García-Berrocal JR, Nevado J, Ramírez-Camacho R, Sanz R, González-García JA, Sánchez-Rodríguez C, Cantos B, España P, Verdaguer JM, Trinidad Cabezas A (2007) Antitumoral drug cisplatin induces an intrinsic apoptotic pathway inside the inner ear. British J Pharmacol 152:1012–1020CrossRef

27.

Wang J, Ladrech S, Pujol R, Brabet P, Van de Water RT, Puel JL (2004) Caspase inhibitors, but not c-Jun NH-N-terminal kinase inhibitor treatment, prevent cisplatin-induced hearing loss. Cancer Res 64:9217–9224

28.

Jeong HJ, Choi Y, Kim MH, Kang IC, Lee JH, Park C, Park R, Kim HM (2011) Rosmarinic acid, active component of Dansam-Eum attenuates ototoxicity of cochlear hair cells through blockage of caspase-1 activity. PLoS ONE 6(4):e18815PubMedCrossRef

29.

So H, Kim H, Kim Y, Kim E, Pae HO, Chung HT, Kim HJ, Kwon KB, Lee KM, Lee HY, Moon SK, Park R (2008) Evidence that cisplatin-induced auditory damage is attenuated by downregulation of pro-inflammatory cytokines via Nrf2/HO-1. J Assoc Res Otolaryngol 9:290–306PubMedCrossRef

30.

Watanabe K, Inai S, Jinnouchi K, Bada S, Hess A, Michel O, Yagi T (2002) Nuclear-factor kappa B (NF-kB)-inducible nitric oxide synthase (iNOS/NOS II) pathway damages the stria vascularis in cisplatin-treated mice. Anticancer Res 22:4081–4085PubMed

31.

So H, Kim H, Lee JH, Park C, Kim Y, Kim E, Kim JK, Yun KJ, Lee KM, Lee HY, Moon SK, Lim DJ, Park R (2007) Cisplatin cytotoxicity of auditory cells requires secretions of proinflammatory cytokines via activation of ERK and NF-kB. J Assoc Res Otolaryngol 8:338–355PubMedCrossRef

32.

Kaur T, Mukherjea D, Sheehan K, Jajoo S, Rybak LP, Ramkumar V (2011) Short interfering RNA against STAT1 attenuates cisplatin-induced ototoxicity in the rat by suppressing inflammation. Cell Death Dis 2:e180PubMedCrossRef

Title: Reactive oxygen species in apoptosis induced by cisplatin: review of physiopathological mechanisms in animal models
Authors: Celia Casares
Rafael Ramírez-Camacho
Almudena Trinidad
Amaya Roldán
Eduardo Jorge
José Ramón García-Berrocal
Publication date: 01-12-2012
Publisher: Springer-Verlag
Published in: European Archives of Oto-Rhino-Laryngology / Issue 12/2012
Print ISSN: 0937-4477
Electronic ISSN: 1434-4726
DOI: https://doi.org/10.1007/s00405-012-2029-0

At a glance: The STEP trials

Springer Medicine

Reactive oxygen species in apoptosis induced by cisplatin: review of physiopathological mechanisms in animal models

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 12/2012

Septal perforation repair: mucosal regeneration technique

Hepatitis C virus in patients with squamous cell carcinoma of the head and neck in Iran: is there any relation?

Lower lip reconstruction with Abbe–Estlander flap modification: preserving the same side vascular pedicle

The impact of cidofovir treatment on viral loads in adult recurrent respiratory papillomatosis

Behcet’s disease impairs voice quality without laryngeal and hypopharyngeal involvement

The relationship between Th1/Th2 balance and 1α,25-dihydroxyvitamin D3 in patients with nasal polyposis