Ototoxic drugs: difference in sensitivity between mice and guinea pigs.

Animals; Anti-Bacterial Agents/toxicity; Antineoplastic Agents/toxicity; Cisplatin/toxicity; Deafness/chemically induced/pathology; Drug Toxicity; Evoked Potentials, Auditory, Brain Stem/drug effects; Fluorescent Antibody Technique; Guinea Pigs; Hearing/drug effects; Kanamycin/toxicity; Male; Mice; Mice, Inbred BALB C; Neurons/pathology; Organ of Corti/pathology; Species Specificity; Spiral Ganglion/drug effects/pathology; Tolonium Chloride

Abstract :

[en] The development of experimental animal models has played an invaluable role in understanding the mechanisms of neurosensory deafness and in devising effective treatments. The purpose of this study was to develop an adult mouse model of ototoxic drug-induced hearing loss and to compare the ototoxicity in the adult mouse to that in the well-described guinea pig model. Mice are a powerful model organism, especially due to the large availability of antibodies, probes and genetic mutants. In this study, mice (n=114) and guinea pigs (n=35) underwent systemic treatment with either kanamycin or cisplatin. Auditory brainstem responses showed a significant threshold shift in guinea pigs 2 weeks after the beginning of the ototoxic treatment, while there was no significant hearing impairment recorded in mice. Hair cells and neuronal loss were correlated with hearing function in both guinea pigs and mice. These results indicate that the mouse is not a good model for ototoxicity, which should be taken into consideration in all further investigations concerning ototoxicity-induced hearing loss.

Research center :

Giga-Neurosciences - ULiège

Disciplines :

Otolaryngology
Biochemistry, biophysics & molecular biology
Biotechnology

Author, co-author :

Poirrier, Anne-Lise ; Centre Hospitalier Universitaire de Liège - CHU > O.R.L.

Van Den Ackerveken, Priscilla

Kim, T. S.

Vandenbosch, Renaud ; Université de Liège - ULiège > GIGA - Neurosciences

Nguyen, Laurent ; Université de Liège - ULiège > Département des sciences cliniques > Neurologie

Lefèbvre, Philippe ; Université de Liège - ULiège > Département des sciences cliniques > Oto-rhino-laryngologie et audiophonologie

Malgrange, Brigitte ; Université de Liège - ULiège > GIGA - Neurosciences - Neurologie

Language :

English

Title :

Ototoxic drugs: difference in sensitivity between mice and guinea pigs.

Publication date :

2010

Journal title :

Toxicology Letters

ISSN :

0378-4274

eISSN :

1879-3169

Publisher :

Elsevier, Amsterdam, Netherlands

Volume :

193

Issue :

Pages :

41-9

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]
Fonds Léon Fredericq [BE]

Available on ORBi :

since 29 January 2010

Statistics

Number of views

155 (28 by ULiège)

Number of downloads

9 (7 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Anniko M. Principles in cochlear toxicity. Arch. Toxicol. Suppl. 8 (1985) 221-239
Aran J.M., Erre J.P., Lima da C.D., Debbarh I., and Dulon D. Acute and chronic effects of aminoglycosides on cochlear hair cells. Ann. N.Y. Acad. Sci. 884 (1999) 60-68
Banfi B., Malgrange B., Knisz J., Steger K., Dubois-Dauphin M., and Krause K.H. NOX3, a superoxide-generating NADPH oxidase of the inner ear. J. Biol. Chem. 279 (2004) 46065-46072
Billings K.R., and Kenna M.A. Causes of pediatric sensorineural hearing loss: yesterday and today. Arch. Otolaryngol. Head Neck Surg. 125 (1999) 517-521
Blakley B.W., Hochman J., Wellman M., Gooi A., and Hussain A.E. Differences in ototoxicity across species. J. Otolaryngol. Head Neck Surg. 37 (2008) 700-703
Bock G.R., Yates G.K., Miller J.J., and Moorjani P. Effects of N-acetylcysteine on kanamycin ototoxicity in the guinea pig. Hear. Res. 9 (1983) 255-262
Bowers W.J., Chen X., Guo H., Frisina D.R., Federoff H.J., and Frisina R.D. Neurotrophin-3 transduction attenuates cisplatin spiral ganglion neuron ototoxicity in the cochlea. Mol. Ther. 6 (2002) 12-18
Brown S.D., Hardisty-Hughes R.E., and Mburu P. Quiet as a mouse: dissecting the molecular and genetic basis of hearing. Nat. Rev. Genet. 9 (2008) 277-290
Church M.W., Blakley B.W., Burgio D.L., and Gupta A.K. WR-2721 (Amifostine) ameliorates cisplatin-induced hearing loss but causes neurotoxicity in hamsters: dose-dependent effects. J. Assoc. Res. Otolaryngol. 5 (2004) 227-237
Conlon B.J., and Smith D.W. Supplemental iron exacerbates aminoglycoside ototoxicity in vivo. Hear. Res. 115 (1998) 1-5
Dai C.F., Mangiardi D., Cotanche D.A., and Steyger P.S. Uptake of fluorescent gentamicin by vertebrate sensory cells in vivo. Hear. Res. 213 (2006) 64-78
Dai C.F., and Steyger P.S. A systemic gentamicin pathway across the stria vascularis. Hear. Res. 235 (2008) 114-124
Dickey D.T., Wu Y.J., Muldoon L.L., and Neuwelt E.A. Protection against cisplatin-induced toxicities by N-acetylcysteine and sodium thiosulfate as assessed at the molecular, cellular, and in vivo levels. J. Pharmacol. Exp. Ther. 314 (2005) 1052-1058
Farris F.F., Dedrick R.L., and King F.G. Cisplatin pharmacokinetics: applications of a physiological model. Toxicol. Lett. 43 (1988) 117-137
Feldman L., Efrati S., Eviatar E., Abramsohn R., Yarovoy I., Gersch E., Averbukh Z., and Weissgarten J. Gentamicin-induced ototoxicity in hemodialysis patients is ameliorated by N-acetylcysteine. Kidney Int. 72 (2007) 359-363
Fetoni A.R., Sergi B., Ferraresi A., Paludetti G., and Troiani D. alpha-Tocopherol protective effects on gentamicin ototoxicity: an experimental study. Int. J. Audiol. 43 (2004) 166-171
Fetoni A.R., Sergi B., Ferraresi A., Paludetti G., and Troiani D. Protective effects of alpha-tocopherol and tiopronin against cisplatin-induced ototoxicity. Acta Otolaryngol. 124 (2004) 421-426
Fetoni A.R., Sergi B., Scarano E., Paludetti G., Ferraresi A., and Troiani D. Protective effects of alpha-tocopherol against gentamicin-induced oto-vestibulo toxicity: an experimental study. Acta Otolaryngol. 123 (2003) 192-197
Forge A., and Schacht J. Aminoglycoside antibiotics. Audiol. Neurootol. 5 (2000) 3-22
Gooi A., Hochman J., Wellman M., Blakley L., and Blakley B.W. Ototoxic effects of single-dose versus 19-day daily-dose gentamicin. J. Otolaryngol Head Neck Surg. 37 (2008) 664-667
Hamre K., Tharp R., Poon K., Xiong X., and Smeyne R.J. Differential strain susceptibility following 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) administration acts in an autosomal dominant fashion: quantitative analysis in seven strains of Mus musculus. Brain Res. 828 (1999) 91-103
Hartman B.H., Basak O., Nelson B.R., Taylor V., Bermingham-McDonogh O., and Reh T.A. Hes5 Expression in the Postnatal and Adult Mouse Inner Ear and the Drug-Damaged Cochlea. J. Assoc. Res. Otolaryngol (2009)
Hellberg V., Wallin I., Eriksson S., Hernlund E., Jerremalm E., Berndtsson M., Eksborg S., Arner E.S., Shoshan M., Ehrsson H., and Laurell G. Cisplatin and oxaliplatin toxicity: importance of cochlear kinetics as a determinant for ototoxicity. J. Natl. Cancer Inst. 101 (2009) 37-47
Hill G.W., Morest D.K., and Parham K. Cisplatin-induced ototoxicity: effect of intratympanic dexamethasone injections. Otol. Neurotol. 29 (2008) 1005-1011
Huang C.M. A comparative study of the brain stem auditory response in mammals. Brain Res. 184 (1980) 215-219
Humes H.D. Insights into ototoxicity. Analogies to nephrotoxicity. Ann. N. Y. Acad. Sci. 884 (1999) 15-18
Jiang H., Sha S.H., Forge A., and Schacht J. Caspase-independent pathways of hair cell death induced by kanamycin in vivo. Cell. Death Differ. 13 (2006) 20-30
Jiang H., Sha S.H., and Schacht J. NF-kappaB pathway protects cochlear hair cells from aminoglycoside-induced ototoxicity. J. Neurosci. Res. 79 (2005) 644-651
Jiang H., Sha S.H., and Schacht J. Kanamycin alters cytoplasmic and nuclear phosphoinositide signaling in the organ of Corti in vivo. J. Neurochem. 99 (2006) 269-276
Jiang H., Sha S.H., and Schacht J. Rac/Rho pathway regulates actin depolymerization induced by aminoglycoside antibiotics. J. Neurosci. Res. 83 (2006) 1544-1551
Kahn C.M. The Merck Veterinary Manual (2007)
Kalkanis J.G., Whitworth C., and Rybak L.P. Vitamin E reduces cisplatin ototoxicity. Laryngoscope 114 (2004) 538-542
King F.G., Dedrick R.L., and Farris F.F. Physiological pharmacokinetic modeling of cis-dichlorodiammineplatinum(II) (DDP) in several species. J. Pharmacokinet. Biopharm. 14 (1986) 131-155
Kitahara T., Li H.S., and Balaban C.D. Changes in transient receptor potential cation channel superfamily V (TRPV) mRNA expression in the mouse inner ear ganglia after kanamycin challenge. Hear. Res. 201 (2005) 132-144
Kitahara T., Li-Korotky H.S., and Balaban C.D. Regulation of mitochondrial uncoupling proteins in mouse inner ear ganglion cells in response to systemic kanamycin challenge. Neuroscience. 135 (2005) 639-653
Lataye R., Campo P., Pouyatos B., Cossec B., Blachere V., and Morel G. Solvent ototoxicity in the rat and guinea pig. Neurotoxicol. Teratol. 25 (2003) 39-50
Laurell G., Ekborn A., Viberg A., and Canlon B. Effects of a single high dose of cisplatin on the melanocytes of the stria vascularis in the guinea pig. Audiol. Neurootol. 12 (2007) 170-178
Lautermann J., McLaren J., and Schacht J. Glutathione protection against gentamicin ototoxicity depends on nutritional status. Hear. Res. 86 (1995) 15-24
Lautermann J., Song B., McLaren J., and Schacht J. Diet is a risk factor in cisplatin ototoxicity. Hear. Res. 88 (1995) 47-53
Leonova E.V., and Raphael Y. Organization of cell junctions and cytoskeleton in the reticular lamina in normal and ototoxically damaged organ of Corti. Hear. Res. 113 (1997) 14-28
Li G., Frenz D.A., Brahmblatt S., Feghali J.G., Ruben R.J., Berggren D., Arezzo J., and Van De Water T.R. Round window membrane delivery of l-methionine provides protection from cisplatin ototoxicity without compromising chemotherapeutic efficacy. Neurotoxicology 22 (2001) 163-176
Liu Y.H., Ke X.M., Qin Y., Gu Z.P., and Xiao S.F. Adeno-associated virus-mediated Bcl-xL prevents aminoglycoside-induced hearing loss in mice. Chin. Med. J. (Engl) 120 (2007) 1236-1240
Meza G., and Aguilar-Maldonado B. Streptomycin action to the mammalian inner ear vestibular organs: comparison between pigmented guinea pigs and rats. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 146 (2007) 203-206
Minami S.B., Sha S.H., and Schacht J. Antioxidant protection in a new animal model of cisplatin-induced ototoxicity. Hear. Res. 198 (2004) 137-143
Misra M., Rodriguez R.E., North S.L., and Kasprzak K.S. Nickel-induced renal lipid peroxidation in different strains of mice: concurrence with nickel effect on antioxidant defense systems. Toxicol. Lett. 58 (1991) 121-133
Morzaria S., Westerberg B.D., and Kozak F.K. Systematic review of the etiology of bilateral sensorineural hearing loss in children. Int. J. Pediatr. Otorhinolaryngol. 68 (2004) 1193-1198
Oesterle E.C., Campbell S., Taylor R.R., Forge A., and Hume C.R. Sox2 and Jagged1 Expression in Normal and Drug-Damaged Adult Mouse Inner Ear. J. Assoc. Res. Otolaryngol. (2007)
Peng Y.G., Clayton E.C., Means L.W., and Ramsdell J.S. Repeated independent exposures to domoic acid do not enhance symptomatic toxicity in outbred or seizure-sensitive inbred mice. Fundam. Appl. Toxicol. 40 (1997) 63-67
Perera P.Y., Lichy J.H., Mastropaolo J., Rosse R.B., and Deutsch S.I. Expression of NR1, NR2A and NR2B NMDA receptor subunits is not altered in the genetically-inbred Balb/c mouse strain with heightened behavioral sensitivity to MK-801, a noncompetitive NMDA receptor antagonist. Eur. Neuropsychopharmacol. 18 (2008) 814-819
Prestayko A.W., Cadiz M., and Crooke S.T. Incompatibility of aluminum-containing iv administration equipment with cis-dichlorodiammineplatinum(II) administration. Cancer Treat. Rep. 63 (1979) 2118-2119
Rizzi M.D., and Hirose K. Aminoglycoside ototoxicity. Curr. Opin. Otolaryngol. Head Neck Surg. 15 (2007) 352-357
Rybak L.P. Mechanisms of cisplatin ototoxicity and progress in otoprotection. Curr. Opin. Otolaryngol. Head Neck Surg. 15 (2007) 364-369
Rybak L.P., and Whitworth C.A. Ototoxicity: therapeutic opportunities. Drug Discov. Today 10 (2005) 1313-1321
Rybak L.P., Whitworth C.A., Mukherjea D., and Ramkumar V. Mechanisms of cisplatin-induced ototoxicity and prevention. Hear. Res. 226 (2007) 157-167
Schacht J. Biochemistry and pharmacology of aminoglycoside-induced hearing loss. Acta Physiol. Pharmacol. Ther. Latinoam 49 (1999) 251-256
Schauwecker P.E., and Steward O. Genetic determinants of susceptibility to excitotoxic cell death: implications for gene targeting approaches. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 4103-4108
Sergi B., Fetoni A.R., Ferraresi A., Troiani D., Azzena G.B., Paludetti G., and Maurizi M. The role of antioxidants in protection from ototoxic drugs. Acta Otolaryngol. Suppl. (2004) 42-45
Severinsen S.A., Kirkegaard M., and Nyengaard J.R. 2,3-Dihydroxybenzoic acid attenuates kanamycin-induced volume reduction in mouse utricular type I hair cells. Hear. Res. 212 (2006) 99-108
Sha S.H., and Schacht J. Antioxidants attenuate gentamicin-induced free radical formation in vitro and ototoxicity in vivo: d-methionine is a potential protectant. Hear. Res. 142 (2000) 34-40
So H., Kim H., Kim Y., Kim E., Pae H.O., Chung H.T., Kim H.J., Kwon K.B., Lee K.M., Lee H.Y., Moon S.K., and Park R. Evidence that Cisplatin-induced Auditory Damage is Attenuated by Downregulation of Pro-inflammatory Cytokines Via Nrf2/HO-1. J. Assoc. Res. Otolaryngol. (2008)
Staecker H., Praetorius M., Baker K., and Brough D.E. Vestibular hair cell regeneration and restoration of balance function induced by math1 gene transfer. Otol. Neurotol. 28 (2007) 223-231
Swan E.E., Mescher M.J., Sewell W.F., Tao S.L., and Borenstein J.T. Inner ear drug delivery for auditory applications. Adv. Drug Deliv. Rev. 60 (2008) 1583-1599
Taleb M., Brandon C.S., Lee F.S., Harris K.C., Dillmann W.H., and Cunningham L.L. Hsp70 inhibits aminoglycoside-induced hearing loss and cochlear hair cell death. Cell. Stress Chaperones. (2009)
Taylor R.R., Nevill G., and Forge A. Rapid Hair Cell Loss: A Mouse Model for Cochlear Lesions. J. Assoc. Res. Otolaryngol. (2007)
Tepel M. N-acetylcysteine in the prevention of ototoxicity. Kidney Int. 72 (2007) 231-232
Teranishi M., Nakashima T., and Wakabayashi T. Effects of alpha-tocopherol on cisplatin-induced ototoxicity in guinea pigs. Hear. Res. 151 (2001) 61-70
Tran Ba Huy P., Bernard P., and Schacht J. Kinetics of gentamicin uptake and release in the rat. Comparison of inner ear tissues and fluids with other organs. J. Clin. Invest. 77 (1986) 1492-1500
Unal O.F., Ghoreishi S.M., Atas A., Akyurek N., Akyol G., and Gursel B. Prevention of gentamicin induced ototoxicity by trimetazidine in animal model. Int. J. Pediatr. Otorhinolaryngol. 69 (2005) 193-199
van Ruijven M.W., de Groot J.C., Klis S.F., and Smoorenburg G.F. The cochlear targets of cisplatin: an electrophysiological and morphological time-sequence study. Hear. Res. 205 (2005) 241-248
van Ruijven M.W., de Groot J.C., and Smoorenburg G.F. Time sequence of degeneration pattern in the guinea pig cochlea during cisplatin administration. A quantitative histological study. Hear. Res. 197 (2004) 44-54
Walton K., Dorne J.L., and Renwick A.G. Species-specific uncertainty factors for compounds eliminated principally by renal excretion in humans. Food Chem. Toxicol. 42 (2004) 261-274
Wang A.M., Sha S.H., Lesniak W., and Schacht J. Tanshinone (Salviae miltiorrhizae extract) preparations attenuate aminoglycoside-induced free radical formation in vitro and ototoxicity in vivo. Antimicrob. Agents Chemother. 47 (2003) 1836-1841
Wang Q., and Steyger P.S. Trafficking of systemic fluorescent gentamicin into the cochlea and hair cells. J. Assoc. Res. Otolaryngol. (2009)
Wu W.J., Sha S.H., McLaren J.D., Kawamoto K., Raphael Y., and Schacht J. Aminoglycoside ototoxicity in adult CBA, C57BL and BALB mice and the Sprague-Dawley rat. Hear. Res. 158 (2001) 165-178
Yang B., and Bankir L. Urea and urine concentrating ability: new insights from studies in mice. Am. J. Physiol. Renal Physiol. 288 (2005) F881-F896
Zhou X., Jen P.H., Seburn K.L., Frankel W.N., and Zheng Q.Y. Auditory brainstem responses in 10 inbred strains of mice. Brain Res. (2006)